Proteomic changes of aryl hydrocarbon receptor (AhR)-silenced porcine granulosa cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)
Autoři:
Karina Orlowska aff001; Sylwia Swigonska aff002; Agnieszka Sadowska aff001; Monika Ruszkowska aff001; Anna Nynca aff002; Tomasz Molcan aff001; Agata Zmijewska aff001; Renata E. Ciereszko aff001
Působiště autorů:
Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego, Olsztyn, Poland
aff001; Laboratory of Molecular Diagnostics, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Prawochenskiego, Olsztyn, Poland
aff002
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223420
Souhrn
2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) is a toxic man-made chemical compound contaminating the environment and affecting human/animal health and reproduction. Intracellular TCDD action usually involves the activation of aryl hydrocarbon receptor (AhR). The aim of the current study was to examine TCDD-induced changes in the proteome of AhR-silenced porcine granulosa cells. The AhR-silenced cells were treated with TCDD (100 nM) for 3, 12 or 24 h. Total protein was isolated, labeled with cyanines and next, the samples were separated by isoelectric focusing and SDS-PAGE. Proteins of interest were identified by MALDI-TOF/TOF mass spectrometry (MS) analysis and confirmed by western blotting and fluorescence immunocytochemistry. The AhR-targeted siRNA transfection reduced the granulosal expression level of AhR by 60–70%. In AhR-silenced porcine granulosa cells, TCDD influenced the abundance of only three proteins: annexin V, protein disulfide isomerase and ATP synthase subunit beta. The obtained results revealed the ability of TCDD to alter protein abundance in an AhR-independent manner. This study offers a new insight into the mechanism of TCDD action and provide directions for future functional studies focused on molecular effects exerted by TCDD.
Klíčová slova:
Gene expression – Small interfering RNAs – Transfection – Apoptosis – Proteomes – Untranslated regions – Granulosa cells – Propidium iodide staining
Zdroje
1. Larsen JC. Risk assessments of polychlorinated dibenzo- p-dioxins, polychlorinated dibenzofurans, and dioxin-like polychlorinated biphenyls in food. Mol Nutr Food Res. 2006; 50: 885–896. doi: 10.1002/mnfr.200500247 17009211
2. Kulkarni PS, Crespo JG, Afonso CAM. Dioxins sources and current remediation technologies–a review. Environ Int. 2008; 34: 139–153. doi: 10.1016/j.envint.2007.07.009 17826831
3. Milbrath MO, Wenger Y, Chang CW, Emond C, Garabrant D, Gillespie BWet al. Apparent half-lives of dioxins, furans, and polychlorinated biphenyls as a function of age, body fat, smoking status, and breast-feeding. Environ Health Perspect. 2009; 117(3): 417–425. doi: 10.1289/ehp.11781 19337517
4. Beischlag TV, Morales JL, Brett D, Hollingshead BD, Perdew GH. The aryl hydrocarbon receptor complex and the control of gene expression. Crit Rev Eukaryot Gene. 2008; 18(3): 207–250.
5. Denison MS, Soshilov AA, He G, DeGroot DE, Zhao B. Exactly the same but different: promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicol Sci. 2011; 124(1): 1–22. doi: 10.1093/toxsci/kfr218 21908767
6. Mulero-Navarro S and Fernandez-Salguero P.M. New Trends in Aryl Hydrocarbon Receptor Biology. Front Cell Dev Biol. 2016; 11 (4): 45.
7. Wang Y M, Ong S S, Chai S C, Chen T. Role of CAR and PXR in xenobiotic sensing and metabolism. Expert Opin Drug Metab Toxicol. 2012; 8: 803–817. doi: 10.1517/17425255.2012.685237 22554043
8. Swedenborg E, Pongratz I. AhR and ARNT modulate ER signaling. Toxicology. 2010; 268: 132–138. doi: 10.1016/j.tox.2009.09.007 19778576
9. Ghotbaddini M and Powell JB. The AhR Ligand, TCDD, Regulates Androgen Receptor Activity Differently in Androgen-Sensitive versus Castration-Resistant Human Prostate Cancer Cells. Int J Environ Res Public Health. 2015; 12(7): 7506–7518. doi: 10.3390/ijerph120707506 26154658
10. Verma G, Khan MF, Shaquiquzzaman M. Akhtar W, Akhter M, Hasan SMet al. Molecular interactions of dioxins and DLCs with the xenosensors (PXR and CAR): An in silico risk assessment approach. J Mol Recognit. 2017; 30 (12).
11. Khan MF, Alam MM, Verma G, Akhtar W, Rizvi MA, Ali A et al. Molecular Interactions of Dioxins and DLCs with the Ketosteroid Receptors: An in silico Risk Assessment Approach. Toxicol Mech Methods. 2017; 27(2): 151–163. doi: 10.1080/15376516.2016.1273423 27997270
12. Matsumura F. Nongenomic Route of Action of TCDD: Identity, Characteristics, and Toxicological Significance in The AH Receptor in Biology and Toxicology (ed. Pohjanvirta R.) 197–215 (John Wiley & Sons, 2012).
13. Lucie Larigot L, Juricek L, Dairou J, Coumoul X. AhR signaling pathways and regulatory functions. Biochim Open. 2018; 7: 1–9. doi: 10.1016/j.biopen.2018.05.001 30003042
14. Pieklo R, Grochowalski A, Gregoraszczuk EL. 2,3,7,8-tetrachlorodibenzo-p-dioxin alters follicular steroidogenesis in time- and cell-specific manner. Exp Clin Endocr Diab. 2000; 108: 299–304.
15. Grochowalski A, Chrzaszcz R, Pieklo R, Gregoraszczuk EL. Estrogenic and antiestrogenic effect of in vitro treatment of follicular cells with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Chemosphere. 2001; 43: 823–827. doi: 10.1016/s0045-6535(00)00440-9 11372872
16. Gregoraszczuk EL. Dioxin exposure and porcine reproductive hormonal activity. Cad Saude Publ. 2002; 18: 453–462.
17. Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001; 121: 647–653. 11427152
18. Jablonska O, Piasecka J, Ostrowska M, Sobocinska N, Wasowska B, Ciereszko RE. The expression of the aryl hydrocarbon receptor in reproductive and neuroendocrine tissues during the estrus cycle in the pig. Anim Reprod Sci. 2011; 126: 221–228. doi: 10.1016/j.anireprosci.2011.05.010 21715111
19. Sadowska A, Nynca A, Ruszkowska M, Paukszto L, Myszczynski K, Orlowska K, et al. Transcriptional profiling of porcine granulosa cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Chemosphere. 2017; 178: 368–377. doi: 10.1016/j.chemosphere.2017.03.055 28340459
20. Ruszkowska M, Nynca A, Paukszto L, Sadowska A, Swigonska S, Orlowska K, et al. Identification and characterization of long non-coding RNAs in porcine granulosa cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Anim Sci Biotechnol. 2018; 9: 72. doi: 10.1186/s40104-018-0288-3 30338064
21. Orlowska K, Swigonska S, Sadowska A, Ruszkowska M, Nynca A, Molcan T, et al. The effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the proteome of porcine granulosa cells. Chemosphere 2018; 212: 170–181. doi: 10.1016/j.chemosphere.2018.08.046 30144678
22. Sadowska A, Nynca A, Korzeniewska M, Piasecka-Srader J, Jablonska M, Orlowska K, et al. Characterization of porcine granulosa cell line AVG-16. Folia Biol-Prague. 2015; 61: 184–194.
23. Horisberger MA. A method for prolonged survival of primary cell lines. In Vitro Cell Dev Biol Anim. 2006; 42: 143–148. doi: 10.1290/0511081.1 16848633
24. Gregoraszczuk EL, Wójtowicz AK, Zabielny E, Grochowalski A. Dose-and-time dependent effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on progesterone secretion by porcine luteal cells cultured in vitro. J Physiol Pharmacol 2000; 51: 127–135. 10768856
25. Jablonska O, Piasecka-Srader J, Nynca A, Kołomycka A, Robak A, Wąsowska B, et al. 2,3,7,8-tetrachlorodibenzo-p-dioxin alters steroid secretion but does not affect cell viability and the incidence of apoptosis in porcine luteinised granulosa cells. Acta Vet Hung. 2014; 62: 408–421. doi: 10.1556/AVet.2014.015 25038954
26. Sweeney MH, Mocarelli P. Human health effects after exposure to 2,3,7,8-TCDD. Food Addit Contam. 2000; 17(4): 303–316. doi: 10.1080/026520300283379 10912244
27. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007; 8(2): R19. doi: 10.1186/gb-2007-8-2-r19 17291332
28. Ramagli L, Rodriguez L. Quantitation of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis. 1985; 6: 559–563.
29. Tijet N, Boutros PC, Moffat ID, Okey AB, Tuomisto J, Pohjanvirta R. Aryl hydrocarbon receptor regulates distinct dioxin-dependent and dioxin-independent gene batteries. Mol Pharmacol. 2006; 69: 140–153. doi: 10.1124/mol.105.018705 16214954
30. Boutros PC, Bielefeld KA, Pohjanvirta R, Harper PA. Dioxin-dependent and dioxin-independent gene batteries: comparison of liver and kidney in AHR-null mice. Toxicol Sci. 2009; 112: 245–256. doi: 10.1093/toxsci/kfp191 19759094
31. Yoshimori T, Semba T, Takemoto H, Akagi S, Yamamoto A, Tashiro Y. Protein disulfide-isomerase in rat exocrine pancreatic cells is exported from the endoplasmic reticulum despite possessing the retention signal. J Biol Chem. 1990; 265: 15984–15990. 2394756
32. Ali Khan H, Mutus B. Protein disulfide isomerase a multifunctional protein with multiple physiological roles. Front Chem. 2014; 2: 70. doi: 10.3389/fchem.2014.00070 25207270
33. Macer DR, Koch GL. Identification of a set of calcium-binding proteins in reticuloplasm, the luminal content of the endoplasmic reticulum. J Cell Sci. 1988; 91: 61–70. 3253304
34. Lebeche D, Lucero HA, Kaminer B. Calcium binding properties of rabbit liver protein disulfide isomerase. Biochem Biophys Res Commun. 1994; 202: 556–561. doi: 10.1006/bbrc.1994.1964 8037762
35. Coe H, Michalak M. Calcium binding chaperones of the endoplasmic reticulum. Gen Physiol Biophys. 2009; 28: 96–103.
36. Puga A, Hoffer A, Zhou S, Bohm JM, Leikauf GD, Shertzer HG. Sustained increase in intracellular free calcium and activation of cyclooxygenase-2 expression in mouse hepatoma cells treated with dioxin. Biochem Pharmacol. 1997; 54: 1287–1296. doi: 10.1016/s0006-2952(97)00417-6 9393671
37. Mayati A, Le Ferrec E, Lagadic-Gossmann D, Fardel O. Aryl hydrocarbon receptor-independent up regulation of intracellular calcium concentration by environmental polycyclic aromatic hydrocarbons in human endothelial HMEC-1 cells. Environ Toxicol. 2012; 27: 556–562. doi: 10.1002/tox.20675 21452393
38. Shertzer HG, Genter MB, Shen D, Nebert DW, Chen Y, Dalton TP. TCDD decreases ATP levels and increases reactive oxygen production through changes in mitochondrial F(0)F(1)-ATP synthase and ubiquinone. Toxicol Appl Pharmacol. 2006; 217: 363–374. doi: 10.1016/j.taap.2006.09.014 17109908
39. Chen SC, Liao TL, Wei YH, Tzeng CR, Kao SH. Endocrine disruptor, dioxin (TCDD) induced mitochondrial dysfunction and apoptosis in humantrophoblast-like JAR cells. Mol Hum Reprod. 2010; 16: 361–372. doi: 10.1093/molehr/gaq004 20083559
40. Comelli M, Di Pancrazio F, Mavelli I. Apoptosis is induced by decline of mitochondrial ATP synthesis in erythroleukemia cells. Free Radic Biol Med. 2003; 34: 1190–1199. doi: 10.1016/s0891-5849(03)00107-2 12706499
41. Wolvetang EJ, Johnson KL, Krauer K, Ralph SJ, Linnane AW. Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett. 1994; 339: 40–44. doi: 10.1016/0014-5793(94)80380-3 8313978
42. Marton A, Mihalik R, Bratincsák A, Adleff V, Peták I, Végh M, et al. Apoptotic cell death induced by inhibitors of energy conservation—Bcl-2 inhibits apoptosis downstream of a fall of ATP level. Eur J Biochem. 1997; 250: 467–475. doi: 10.1111/j.1432-1033.1997.0467a.x 9428700
43. Terminella C, Tollefson K, Kroczynski J, Pelli J, Cutaia M. Inhibition of apoptosis in pulmonary endothelial cells by altered pH, mitochondrial function, and ATP supply. Am J Physiol Lung Cell Mol Physiol. 2002; 283: 1291–1302.
44. Onda M, Emi M, Yoshida A, Miyamoto S, Akaishi J, Asaka S, et al. Comprehensive gene expression profiling of anaplastic thyroid cancers with cDNA microarray of 25 344 genes. Endocr Relat Cancer. 2004; 11: 843–854. doi: 10.1677/erc.1.00818 15613457
45. Moss SE, Morgan RO. The annexins. Genome Biol. 2004; 5(4): 219. doi: 10.1186/gb-2004-5-4-219 15059252
46. Gerke V, Creutz CE, Moss SE. Annexins: linking Ca2+ signalling to membrane dynamics. Nat Rev Mol Cell Biol. 2005; 6: 449–461. doi: 10.1038/nrm1661 15928709
47. Boersma HH, Kietselaer BL, Stolk LM, Bennaghmouch A, Hofstra L, Narula J, et al. Past, present, and future of annexin A5: from protein discovery to clinical applications. J Nucl Med. 2005; 46: 2035–2050. 16330568
48. Monastyrskaya K, Babiychuk EB, Hostettler A, Rescher U, Draeger A. Annexins as intracellular calcium sensors. Cell Calcium. 2007; 41: 207–219. doi: 10.1016/j.ceca.2006.06.008 16914198
49. Jeong JJ, Park N, Kwon YJ, Ye DJ, Moon A, Chun YJ. Role of annexin A5 in cisplatin-induced toxicity in renal cells: molecular mechanism of apoptosis. J Biol Chem. 2014; 289: 2469–2481. doi: 10.1074/jbc.M113.450163 24318879
50. Ravassa S, García-Bolao I, Zudaire A, Macías A, Gavira JJ, Beaumont J, et al. Cardiac resynchronization therapy-induced left ventricular reverse remodelling is associated with reduced plasma annexin A5. Cardiovasc Res. 2010; 88: 304–313. doi: 10.1093/cvr/cvq183 20542876
51. Ea HK, Monceau V, Camors E, Cohen-Solal M, Charlemagne D, Lioté F. Annexin 5 overexpression increased articular chondrocyte apoptosis induced by basic calcium phosphate crystals. Ann Rheum Dis. 2008; 67: 1617–1625. doi: 10.1136/ard.2008.087718 18218665
52. Gidon-Jeangirard C, Solito E, Hofmann A, Russo-Marie F, Freyssinet JM, Martínez MC. Annexin V counteracts apoptosis while inducing Ca(2+) influx in human lymphocytic T cells. Biochem Biophys Res Commun. 1999; 265: 709–715. doi: 10.1006/bbrc.1999.1752 10600485
53. Bouter A, Gounou C, Berat R, Tan S, Gallois B, Granier T, d'Estaintot BLet al. Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Nat Commun. 2011; 2: 270. doi: 10.1038/ncomms1270 21468022
54. Carmeille R, Degrelle SA, Plawinski L, Bouvet F, Gounou C, Evain-Brion D, et al. Annexin-A5 promotes membrane resealing in human trophoblasts. Biochim Biophys Acta. 2015; 1853: 2033–2044. doi: 10.1016/j.bbamcr.2014.12.038 25595530
55. Piasecka-Srader J, Sadowska A, Nynca A, Orlowska K, Jablonska M, Jablonska O, et al. The combined effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin and the phytoestrogen genistein on steroid hormone secretion, AhR and ERb expression and the incidence of apoptosis in granulosa cells of medium porcine follicles. J Reprod Develop 2016; 62: 103–113.
Článok vyšiel v časopise
PLOS One
2019 Číslo 10
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Experimentally validated simulation of coronary stents considering different dogboning ratios and asymmetric stent positioning
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis