ATF3 downmodulates its new targets IFI6 and IFI27 to suppress the growth and migration of tongue squamous cell carcinoma cells
Autoři:
Lin Xu aff001; Tingjian Zu aff001; Tao Li aff001; Min Li aff004; Jun Mi aff001; Fuxiang Bai aff001; Guanyi Liu aff001; Jie Wen aff001; Hui Li aff006; Cord Brakebusch aff007; Xuxia Wang aff002; Xunwei Wu aff001
Působiště autorů:
Department of Tissue Engineering and Regeneration, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration and Shandong Engineering Laboratory for Dental Materials and O...
aff001; Department of Oral and Maxillofacial Surgery, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Laboratory for Dental Materials and Oral Tis...
aff002; Department of Orthodontics, Liaocheng People’s Hospital, Liaocheng, Shandong, China
aff003; Precision Biomedical Key Laboratory, Liaocheng People’s Hospital, Liaocheng, Shandong, China
aff004; School of Stomatology, Shandong First Medical University & Shandong Academy of Medical Sciences, Tai’an, Shandong, China
aff005; Department of Hematology, Southwest Hospital, Third Military Medical University, Chongqing, China
aff006; Biotech Research and Innovation Centre (BRIC), University of Copenhagen, Ole Maaløes Vej 5, Copenhagen, Denmark
aff007
Vyšlo v časopise:
ATF3 downmodulates its new targets IFI6 and IFI27 to suppress the growth and migration of tongue squamous cell carcinoma cells. PLoS Genet 17(2): e1009283. doi:10.1371/journal.pgen.1009283
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009283
Souhrn
Activating transcription factor 3 (ATF3) is a key transcription factor involved in regulating cellular stress responses, with different expression levels and functions in different tissues. ATF3 has also been shown to play crucial roles in regulating tumor development and progression, however its potential role in oral squamous cell carcinomas has not been fully explored. In this study, we examined biopsies of tongue squamous cell carcinomas (TSCCs) and found that the nuclear expression level of ATF3 correlated negatively with the differentiation status of TSCCs, which was validated by analysis of the ATGC database. By using gain- or loss- of function analyses of ATF3 in four different TSCC cell lines, we demonstrated that ATF3 negatively regulates the growth and migration of human TSCC cells in vitro. RNA-seq analysis identified two new downstream targets of ATF3, interferon alpha inducible proteins 6 (IFI6) and 27 (IFI27), which were upregulated in ATF3-deleted cells and were downregulated in ATF3-overexpressing cells. Chromatin immunoprecipitation assays showed that ATF3 binds the promoter regions of the IFI6 and IFI27 genes. Both IFI6 and IFI27 were highly expressed in TSCC biopsies and knockdown of either IFI6 or IFI27 in TSCC cells blocked the cell growth and migration induced by the deletion of ATF3. Conversely, overexpression of either IFI6 or IFI27 counteracted the inhibition of TSCC cell growth and migration induced by the overexpression of ATF3. Finally, an in vivo study in mice confirmed those in vitro findings. Our study suggests that ATF3 plays an anti-tumor function in TSCCs through the negative regulation of its downstream targets, IFI6 and IFI27.
Klíčová slova:
Prostate cancer – Breast cancer – Hepatocellular carcinoma – Cancers and neoplasms – Cell migration – Hyperexpression techniques – Nuclear staining – Small interfering RNA
Zdroje
1. Vigneswaran N, Williams MD. Epidemiologic trends in head and neck cancer and aids in diagnosis. Oral Maxillofac Surg Clin North Am. 2014;26(2):123–41. Epub 2014/05/06. doi: 10.1016/j.coms.2014.01.001 24794262; PubMed Central PMCID: PMC4040236.
2. Boldrup L, Coates PJ, Laurell G, Wilms T, Fahraeus R, Nylander K. Downregulation of miRNA-424: a sign of field cancerisation in clinically normal tongue adjacent to squamous cell carcinoma. Br J Cancer. 2015;112(11):1760–5. Epub 2015/05/13. doi: 10.1038/bjc.2015.150 25965165; PubMed Central PMCID: PMC4647232.
3. Hussein AA, Forouzanfar T, Bloemena E, de Visscher J, Brakenhoff RH, Leemans CR, et al. A review of the most promising biomarkers for early diagnosis and prognosis prediction of tongue squamous cell carcinoma. Br J Cancer. 2018;119(6):724–36. Epub 2018/08/23. doi: 10.1038/s41416-018-0233-4 30131545; PubMed Central PMCID: PMC6173763.
4. Karatas OF, Oner M, Abay A, Diyapoglu A. MicroRNAs in human tongue squamous cell carcinoma: From pathogenesis to therapeutic implications. Oral Oncol. 2017;67:124–30. Epub 2017/03/30. doi: 10.1016/j.oraloncology.2017.02.015 28351566.
5. Hai T, Wolford CC, Chang YS. ATF3, a hub of the cellular adaptive-response network, in the pathogenesis of diseases: is modulation of inflammation a unifying component? Gene expression. 2010;15(1):1–11. Epub 2010/11/11. doi: 10.3727/105221610x12819686555015 21061913; PubMed Central PMCID: PMC6043823.
6. Rohini M, Haritha Menon A, Selvamurugan N. Role of activating transcription factor 3 and its interacting proteins under physiological and pathological conditions. Int J Biol Macromol. 2018;120(Pt A):310–7. Epub 2018/08/26. doi: 10.1016/j.ijbiomac.2018.08.107 30144543.
7. Thompson MR, Xu D, Williams BR. ATF3 transcription factor and its emerging roles in immunity and cancer. J Mol Med (Berl). 2009;87(11):1053–60. Epub 2009/08/26. doi: 10.1007/s00109-009-0520-x 19705082; PubMed Central PMCID: PMC2783469.
8. Wang A, Arantes S, Yan L, Kiguchi K, McArthur MJ, Sahin A, et al. The transcription factor ATF3 acts as an oncogene in mouse mammary tumorigenesis. BMC cancer. 2008;8:268. Epub 2008/09/24. doi: 10.1186/1471-2407-8-268 18808719; PubMed Central PMCID: PMC2564979.
9. Park GH, Park JH, Eo HJ, Song HM, Woo SH, Kim MK, et al. The induction of activating transcription factor 3 (ATF3) contributes to anti-cancer activity of Abeliophyllum distichum Nakai in human colorectal cancer cells. BMC complementary and alternative medicine. 2014;14:487. Epub 2014/12/17. doi: 10.1186/1472-6882-14-487 25494848; PubMed Central PMCID: PMC4302050.
10. Wang Z, He Y, Deng W, Lang L, Yang H, Jin B, et al. Atf3 deficiency promotes genome instability and spontaneous tumorigenesis in mice. Oncogene. 2018;37(1):18–27. Epub 2017/09/05. doi: 10.1038/onc.2017.310 28869597; PubMed Central PMCID: PMC6179156.
11. Avraham S, Korin B, Aviram S, Shechter D, Shaked Y, Aronheim A. ATF3 and JDP2 deficiency in cancer associated fibroblasts promotes tumor growth via SDF-1 transcription. Oncogene. 2019;38(20):3812–23. Epub 2019/01/24. doi: 10.1038/s41388-019-0692-y 30670778; PubMed Central PMCID: PMC6756089.
12. Jiang X, Kim KJ, Ha T, Lee SH. Potential Dual Role of Activating Transcription Factor 3 in Colorectal Cancer. Anticancer Res. 2016;36(2):509–16. Epub 2016/02/07. 26851004.
13. Wu X, Nguyen BC, Dziunycz P, Chang S, Brooks Y, Lefort K, et al. Opposing roles for calcineurin and ATF3 in squamous skin cancer. Nature. 2010;465(7296):368–72. Epub 2010/05/21. doi: 10.1038/nature08996 20485437; PubMed Central PMCID: PMC3050632.
14. Dziunycz PJ, Lefort K, Wu X, Freiberger SN, Neu J, Djerbi N, et al. The oncogene ATF3 is potentiated by cyclosporine A and ultraviolet light A. The Journal of investigative dermatology. 2014;134(7):1998–2004. Epub 2014/02/11. doi: 10.1038/jid.2014.77 24509533.
15. Zhao W, Sun M, Li S, Chen Z, Geng D. Transcription factor ATF3 mediates the radioresistance of breast cancer. J Cell Mol Med. 2018;22(10):4664–75. Epub 2018/08/18. doi: 10.1111/jcmm.13688 30117642; PubMed Central PMCID: PMC6156394.
16. Li X, Zhou X, Li Y, Zu L, Pan H, Liu B, et al. Activating transcription factor 3 promotes malignance of lung cancer cells in vitro. Thorac Cancer. 2017;8(3):181–91. Epub 2017/02/28. doi: 10.1111/1759-7714.12421 28239957; PubMed Central PMCID: PMC5415490.
17. Xie JJ, Xie YM, Chen B, Pan F, Guo JC, Zhao Q, et al. ATF3 functions as a novel tumor suppressor with prognostic significance in esophageal squamous cell carcinoma. Oncotarget. 2014;5(18):8569–82. Epub 2014/08/26. doi: 10.18632/oncotarget.2322 25149542; PubMed Central PMCID: PMC4226705.
18. Li J, Yang Z, Chen Z, Bao Y, Zhang H, Fang X, et al. ATF3 suppresses ESCC via downregulation of ID1. Oncol Lett. 2016;12(3):1642–8. Epub 2016/09/08. doi: 10.3892/ol.2016.4832 27602100; PubMed Central PMCID: PMC4998220.
19. Inoue M, Uchida Y, Edagawa M, Hirata M, Mitamura J, Miyamoto D, et al. The stress response gene ATF3 is a direct target of the Wnt/beta-catenin pathway and inhibits the invasion and migration of HCT116 human colorectal cancer cells. PLoS One. 2018;13(7):e0194160. Epub 2018/07/03. doi: 10.1371/journal.pone.0194160 29966001; PubMed Central PMCID: PMC6028230.
20. Chen C, Ge C, Liu Z, Li L, Zhao F, Tian H, et al. ATF3 inhibits the tumorigenesis and progression of hepatocellular carcinoma cells via upregulation of CYR61 expression. J Exp Clin Cancer Res. 2018;37(1):263. Epub 2018/11/01. doi: 10.1186/s13046-018-0919-8 30376856; PubMed Central PMCID: PMC6208028.
21. Wang Z, Yan C. Emerging roles of ATF3 in the suppression of prostate cancer. Mol Cell Oncol. 2016;3(1):e1010948. Epub 2016/06/17. doi: 10.1080/23723556.2015.1010948 27308526; PubMed Central PMCID: PMC4845162.
22. Wang Z, Kim J, Teng Y, Ding HF, Zhang J, Hai T, et al. Loss of ATF3 promotes hormone-induced prostate carcinogenesis and the emergence of CK5(+)CK8(+) epithelial cells. Oncogene. 2016;35(27):3555–64. Epub 2015/11/03. doi: 10.1038/onc.2015.417 26522727; PubMed Central PMCID: PMC4853303.
23. Shi B, Yan W, Liu G, Guo Y. MicroRNA-488 inhibits tongue squamous carcinoma cell invasion and EMT by directly targeting ATF3. Cell Mol Biol Lett. 2018;23:28. Epub 2018/06/28. doi: 10.1186/s11658-018-0094-0 29946339; PubMed Central PMCID: PMC6006839.
24. Hu YT, Li XX, Zeng LW. Circ_0001742 promotes tongue squamous cell carcinoma progression via miR-431-5p/ATF3 axis. Eur Rev Med Pharmacol Sci. 2019;23(23):10300–12. Epub 2019/12/17. doi: 10.26355/eurrev_201912_19668 31841185.
25. Chandrashekar DS, Bashel B, Balasubramanya SAH, Creighton CJ, Ponce-Rodriguez I, Chakravarthi B, et al. UALCAN: A Portal for Facilitating Tumor Subgroup Gene Expression and Survival Analyses. Neoplasia. 2017;19(8):649–58. Epub 2017/07/22. doi: 10.1016/j.neo.2017.05.002 28732212; PubMed Central PMCID: PMC5516091.
26. Vidal P. Interferon alpha in cancer immunoediting: From elimination to escape. Scand J Immunol. 2020;91(5):e12863. Epub 2020/01/08. doi: 10.1111/sji.12863 31909839.
27. Keilwagen J, Posch S, Grau J. Accurate prediction of cell type-specific transcription factor binding. Genome Biol. 2019;20(1):9. Epub 2019/01/12. doi: 10.1186/s13059-018-1614-y 30630522; PubMed Central PMCID: PMC6327544.
28. Gertz J, Savic D, Varley KE, Partridge EC, Safi A, Jain P, et al. Distinct properties of cell-type-specific and shared transcription factor binding sites. Mol Cell. 2013;52(1):25–36. Epub 2013/10/01. doi: 10.1016/j.molcel.2013.08.037 24076218; PubMed Central PMCID: PMC3811135.
29. Zhao J, Li X, Guo M, Yu J, Yan C. The common stress responsive transcription factor ATF3 binds genomic sites enriched with p300 and H3K27ac for transcriptional regulation. BMC Genomics. 2016;17:335. Epub 2016/05/06. doi: 10.1186/s12864-016-2664-8 27146783; PubMed Central PMCID: PMC4857411.
30. Kim DE, Procopio MG, Ghosh S, Jo SH, Goruppi S, Magliozzi F, et al. Convergent roles of ATF3 and CSL in chromatin control of cancer-associated fibroblast activation. J Exp Med. 2017;214(8):2349–68. Epub 2017/07/08. doi: 10.1084/jem.20170724 28684431; PubMed Central PMCID: PMC5551580.
31. Wang H, Qiu X, Lin S, Chen X, Wang T, Liao T. Knockdown of IFI27 inhibits cell proliferation and invasion in oral squamous cell carcinoma. World J Surg Oncol. 2018;16(1):64. Epub 2018/03/28. doi: 10.1186/s12957-018-1371-0 29580248; PubMed Central PMCID: PMC5870725.
32. Heyden A, Huitfeldt HS, Koppang HS, Thrane PS, Bryne M, Brandtzaeg P. Cytokeratins as epithelial differentiation markers in premalignant and malignant oral lesions. J Oral Pathol Med. 1992;21(1):7–11. Epub 1992/01/01. doi: 10.1111/j.1600-0714.1992.tb00960.x 1375644.
33. Bloor BK, Seddon SV, Morgan PR. Gene expression of differentiation-specific keratins in oral epithelial dysplasia and squamous cell carcinoma. Oral Oncol. 2001;37(3):251–61. Epub 2001/04/05. doi: 10.1016/s1368-8375(00)00094-4 11287279.
34. Wang Z, Xu D, Ding HF, Kim J, Zhang J, Hai T, et al. Loss of ATF3 promotes Akt activation and prostate cancer development in a Pten knockout mouse model. Oncogene. 2015;34(38):4975–84. Epub 2014/12/23. doi: 10.1038/onc.2014.426 25531328; PubMed Central PMCID: PMC4476969.
35. Bandyopadhyay S, Wang Y, Zhan R, Pai SK, Watabe M, Iiizumi M, et al. The tumor metastasis suppressor gene Drg-1 down-regulates the expression of activating transcription factor 3 in prostate cancer. Cancer Res. 2006;66(24):11983–90. Epub 2006/12/21. doi: 10.1158/0008-5472.CAN-06-0943 17178897.
36. Wolford CC, McConoughey SJ, Jalgaonkar SP, Leon M, Merchant AS, Dominick JL, et al. Transcription factor ATF3 links host adaptive response to breast cancer metastasis. J Clin Invest. 2013;123(7):2893–906. Epub 2013/08/08. doi: 10.1172/JCI64410 23921126; PubMed Central PMCID: PMC3696548.
37. Wang A, Arantes S, Conti C, McArthur M, Aldaz CM, MacLeod MC. Epidermal hyperplasia and oral carcinoma in mice overexpressing the transcription factor ATF3 in basal epithelial cells. Mol Carcinog. 2007;46(6):476–87. Epub 2007/02/14. 10.1002/mc.20298. doi: 10.1002/mc.20298 17295236.
38. Hunt D, Raivich G, Anderson PN. Activating transcription factor 3 and the nervous system. Front Mol Neurosci. 2012;5:7. Epub 2012/02/22. doi: 10.3389/fnmol.2012.00007 22347845; PubMed Central PMCID: PMC3278981.
39. Lindwall C, Dahlin L, Lundborg G, Kanje M. Inhibition of c-Jun phosphorylation reduces axonal outgrowth of adult rat nodose ganglia and dorsal root ganglia sensory neurons. Mol Cell Neurosci. 2004;27(3):267–79. Epub 2004/11/03. doi: 10.1016/j.mcn.2004.07.001 15519242.
40. Kim JY, Song EH, Lee S, Lim JH, Choi JS, Koh IU, et al. The induction of STAT1 gene by activating transcription factor 3 contributes to pancreatic beta-cell apoptosis and its dysfunction in streptozotocin-treated mice. Cell Signal. 2010;22(11):1669–80. Epub 2010/07/06. doi: 10.1016/j.cellsig.2010.06.007 20600850.
41. Mladinic M, Bianchetti E, Dekanic A, Mazzone GL, Nistri A. ATF3 is a novel nuclear marker for migrating ependymal stem cells in the rat spinal cord. Stem Cell Res. 2014;12(3):815–27. Epub 2014/05/08. doi: 10.1016/j.scr.2014.03.006 24801224.
42. Zhou Q, Kim SH, Perez-Lorenzo R, Liu C, Huang M, Dotto GP, et al. Phenformin Promotes Keratinocyte Differentiation via the Calcineurin/NFAT Pathway. The Journal of investigative dermatology. 2020. Epub 2020/07/04. doi: 10.1016/j.jid.2020.05.114 32619504.
43. Zu T, Wen J, Xu L, Li H, Mi J, Li H, et al. Up-Regulation of Activating Transcription Factor 3 in Human Fibroblasts Inhibits Melanoma Cell Growth and Migration Through a Paracrine Pathway. Front Oncol. 2020;10:624. Epub 2020/05/07. doi: 10.3389/fonc.2020.00624 32373541; PubMed Central PMCID: PMC7187895.
44. Li G, Li X, Yang M, Xu L, Deng S, Ran L. Prediction of biomarkers of oral squamous cell carcinoma using microarray technology. Sci Rep. 2017;7:42105. Epub 2017/02/09. doi: 10.1038/srep42105 28176846; PubMed Central PMCID: PMC5296717.
45. Papac-Milicevic N, Breuss JM, Zaujec J, Ryban L, Plyushch T, Wagner GA, et al. The interferon stimulated gene 12 inactivates vasculoprotective functions of NR4A nuclear receptors. Circ Res. 2012;110(8):e50–63. Epub 2012/03/20. doi: 10.1161/CIRCRESAHA.111.258814 22427340.
46. Xue B, Yang D, Wang J, Xu Y, Wang X, Qin Y, et al. ISG12a Restricts Hepatitis C Virus Infection through the Ubiquitination-Dependent Degradation Pathway. J Virol. 2016;90(15):6832–45. Epub 2016/05/20. doi: 10.1128/JVI.00352-16 27194766; PubMed Central PMCID: PMC4944290.
47. Rosebeck S, Leaman DW. Mitochondrial localization and pro-apoptotic effects of the interferon-inducible protein ISG12a. Apoptosis. 2008;13(4):562–72. Epub 2008/03/12. doi: 10.1007/s10495-008-0190-0 18330707.
48. Gytz H, Hansen MF, Skovbjerg S, Kristensen AC, Horlyck S, Jensen MB, et al. Apoptotic properties of the type 1 interferon induced family of human mitochondrial membrane ISG12 proteins. Biol Cell. 2017;109(2):94–112. Epub 2016/10/27. doi: 10.1111/boc.201600034 27673746.
49. Liu N, Zuo C, Wang X, Chen T, Yang D, Wang J, et al. miR-942 decreases TRAIL-induced apoptosis through ISG12a downregulation and is regulated by AKT. Oncotarget. 2014;5(13):4959–71. Epub 2014/06/28. doi: 10.18632/oncotarget.2067 24970806; PubMed Central PMCID: PMC4148114.
50. Chen Y, Jiao B, Yao M, Shi X, Zheng Z, Li S, et al. ISG12a inhibits HCV replication and potentiates the anti-HCV activity of IFN-alpha through activation of the Jak/STAT signaling pathway independent of autophagy and apoptosis. Virus Res. 2017;227:231–9. Epub 2016/10/26. doi: 10.1016/j.virusres.2016.10.013 27777077.
51. Rawlings JS, Rosler KM, Harrison DA. The JAK/STAT signaling pathway. J Cell Sci. 2004;117(Pt 8):1281–3. Epub 2004/03/17. doi: 10.1242/jcs.00963 15020666.
52. Owen KL, Brockwell NK, Parker BS. JAK-STAT Signaling: A Double-Edged Sword of Immune Regulation and Cancer Progression. Cancers (Basel). 2019;11(12). Epub 2019/12/18. doi: 10.3390/cancers11122031 31888295; PubMed Central PMCID: PMC6966445.
53. Tahara E Jr., Tahara H, Kanno M, Naka K, Takeda Y, Matsuzaki T, et al. G1P3, an interferon inducible gene 6–16, is expressed in gastric cancers and inhibits mitochondrial-mediated apoptosis in gastric cancer cell line TMK-1 cell. Cancer Immunol Immunother. 2005;54(8):729–40. Epub 2005/02/03. doi: 10.1007/s00262-004-0645-2 15685448.
54. Cheriyath V, Glaser KB, Waring JF, Baz R, Hussein MA, Borden EC. G1P3, an IFN-induced survival factor, antagonizes TRAIL-induced apoptosis in human myeloma cells. J Clin Invest. 2007;117(10):3107–17. Epub 2007/09/08. doi: 10.1172/JCI31122 17823654; PubMed Central PMCID: PMC1964509.
55. Qi Y, Li Y, Zhang Y, Zhang L, Wang Z, Zhang X, et al. IFI6 Inhibits Apoptosis via Mitochondrial-Dependent Pathway in Dengue Virus 2 Infected Vascular Endothelial Cells. PLoS One. 2015;10(8):e0132743. Epub 2015/08/06. doi: 10.1371/journal.pone.0132743 26244642; PubMed Central PMCID: PMC4526556.
56. Cheriyath V, Kuhns MA, Jacobs BS, Evangelista P, Elson P, Downs-Kelly E, et al. G1P3, an interferon- and estrogen-induced survival protein contributes to hyperplasia, tamoxifen resistance and poor outcomes in breast cancer. Oncogene. 2012;31(17):2222–36. Epub 2011/10/15. doi: 10.1038/onc.2011.393 21996729.
57. Cheriyath V, Kaur J, Davenport A, Khalel A, Chowdhury N, Gaddipati L. G1P3 (IFI6), a mitochondrial localised antiapoptotic protein, promotes metastatic potential of breast cancer cells through mtROS. Br J Cancer. 2018;119(1):52–64. Epub 2018/06/15. doi: 10.1038/s41416-018-0137-3 29899394; PubMed Central PMCID: PMC6035266.
58. Wu X, Tommasi di Vignano A, Zhou Q, Michel-Dziunycz PJ, Bai F, Mi J, et al. The ARE-binding protein Tristetraprolin (TTP) is a novel target and mediator of calcineurin tumor suppressing function in the skin. PLoS Genet. 2018;14(5):e1007366. Epub 2018/05/04. doi: 10.1371/journal.pgen.1007366 29723192; PubMed Central PMCID: PMC5953486.
59. Liu Z, Wen J, Leng X, Zhou Q, Zhou C, Zhao H, et al. A Simplified and Efficient Method to Isolate Primary Human Keratinocytes from Adult Skin Tissue. J Vis Exp. 2018;(138). Epub 2018/09/11. doi: 10.3791/57784 30199027; PubMed Central PMCID: PMC6231857.
60. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8(11):2281–308. Epub 2013/10/26. doi: 10.1038/nprot.2013.143 24157548; PubMed Central PMCID: PMC3969860.
61. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12:323. Epub 2011/08/06. doi: 10.1186/1471-2105-12-323 21816040; PubMed Central PMCID: PMC3163565.
62. Byadgi O, Chen CW, Wang PC, Tsai MA, Chen SC. De Novo Transcriptome Analysis of Differential Functional Gene Expression in Largemouth Bass (Micropterus salmoides) after Challenge with Nocardia seriolae. Int J Mol Sci. 2016;17(8). Epub 2016/08/17. doi: 10.3390/ijms17081315 27529219; PubMed Central PMCID: PMC5000712.
Článek vyšel v časopise
PLOS Genetics
2021 Číslo 2
- Může hubnutí souviset s vyšším rizikem nádorových onemocnění?
- Raději si zajděte na oční! Jak souvisí citlivost zraku s rozvojem demence?
- Co způsobuje pooperační infekce? Na vině může být i naše vlastní mikrobiota
- Čeká nás průlom v diagnostice karcinomu pankreatu?
- Polibek, který mi „vzal nohy“ aneb vzácný výskyt EBV u 70leté ženy – kazuistika
Nejčtenější v tomto čísle
- Glucocerebrosidase reduces the spread of protein aggregation in a Drosophila melanogaster model of neurodegeneration by regulating proteins trafficked by extracellular vesicles
- ATF3 downmodulates its new targets IFI6 and IFI27 to suppress the growth and migration of tongue squamous cell carcinoma cells
- Transcriptome-wide transmission disequilibrium analysis identifies novel risk genes for autism spectrum disorder
- Four families of folate-independent methionine synthases