Long-Term Effects of Very Low Dose Particle Radiation on Gene Expression in the Heart: Degenerative Disease Risks

Garikipati, Venkata Srikanth; Arakelyan, Arsen; Blakely, Eleanor A.; Chang, Polly Y.; Truongcao, May M.; Cimini, Maria; Malaredy, Vandana; Bajpai, Anamika; Addya, Sankar; Bisserier, Malik; Brojakowska, Agnieszka; Eskandari, Abrisham; Khlgatian, Mary K.; Hadri, Lahouaria; Fish, Kenneth M.; Kishore, Raj; Goukassian, David. A.

doi:10.3390/cells10020387

Long-Term Effects of Very Low Dose Particle Radiation on Gene Expression in the Heart: Degenerative Disease Risks

Journal Article · Sat Feb 13 00:00:00 UTC 2021 · Cells

DOI:https://doi.org/10.3390/cells10020387· OSTI ID:1807569

Garikipati, Venkata Srikanth ^[1]; ^[2]; Blakely, Eleanor A. ^[3]; Chang, Polly Y. ^[4]; Truongcao, May M. ^[5]; Cimini, Maria ^[5]; Malaredy, Vandana ^[5]; Bajpai, Anamika ^[5]; Addya, Sankar ^[6]; ^[7]; ^[7]; ^[7]; Khlgatian, Mary K. ^[7]; Hadri, Lahouaria ^[7]; Fish, Kenneth M. ^[7]; ^[5]; Goukassian, David. A. ^[7]

The Ohio State Univ., Columbus, OH (United States)
PathVerse, Yerevan (Armenia); The National Academy of Sciences of the Republic of Armenia, Yerevan (Armenia)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
SRI International, Menlo Park, CA (United States)
Temple Univ., Philadelphia, PA (United States)
Thomas Jefferson Univ., Philladelphia, PA (United States)
Icahn School of Medicine at Mount Sinai, New York, NY (United States)

Compared to low doses of gamma irradiation (γ-IR), high-charge-and-energy (HZE) particle IR may have different biological response thresholds in cardiac tissue at lower doses, and these effects may be IR type and dose dependent. Three- to four-month-old female CB6F1/Hsd mice were exposed once to one of four different doses of the following types of radiation: γ-IR 137Cs (40-160 cGy, 0.662 MeV), 14Si-IR (4-32 cGy, 260 MeV/n), or 22Ti-IR (3-26 cGy, 1 GeV/n). At 16 months post-exposure, animals were sacrificed and hearts were harvested and archived as part of the NASA Space Radiation Tissue Sharing Forum. These heart tissue samples were used in our study for RNA isolation and microarray hybridization. Functional annotation of twofold up/down differentially expressed genes (DEGs) and bioinformatics analyses revealed the following: (i) there were no clear lower IR thresholds for HZE- or γ-IR; (ii) there were 12 common DEGs across all 3 IR types; (iii) these 12 overlapping genes predicted various degrees of cardiovascular, pulmonary, and metabolic diseases, cancer, and aging; and (iv) these 12 genes revealed an exclusive non-linear DEG pattern in 14Si- and 22Ti-IR-exposed hearts, whereas two-thirds of γ-IR-exposed hearts revealed a linear pattern of DEGs. Thus, our study may provide experimental evidence of excess relative risk (ERR) quantification of low/very low doses of full-body space-type IR-associated degenerative disease development.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

OSTI ID:: 1807569

Alternate ID(s):: OSTI ID: 1810752

Journal Information:: Cells, Journal Name: Cells Journal Issue: 2 Vol. 10; ISSN 2073-4409

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (79)

The CDK domain of p21 is a suppressor of IL-1β-mediated inflammation in activated macrophages: Innate immunity Scatizzi, John C.; Mavers, Melissa; Hutcheson, Jack European Journal of Immunology, Vol. 39, Issue 3 https://doi.org/10.1002/eji.200838683	journal	February 2009
CCAAT/enhancer-binding protein beta (C/EBPβ) knockdown reduces inflammation, ER stress, and apoptosis, and promotes autophagy in oxLDL-treated RAW264.7 macrophage cells Zahid, MD Khurshidul; Rogowski, Michael; Ponce, Christopher Molecular and Cellular Biochemistry, Vol. 463, Issue 1-2 https://doi.org/10.1007/s11010-019-03642-4	journal	November 2019
The crossed nigrostriatal projection decussates in the ventral tegmental decussation Douglas, Rodney; Kellaway, Lauriston; Mintz, Matti Brain Research, Vol. 418, Issue 1 https://doi.org/10.1016/0006-8993(87)90967-X	journal	August 1987
The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases Wade Harper, J. Cell, Vol. 75, Issue 4 https://doi.org/10.1016/0092-8674(93)90499-G	journal	November 1993
Oxy radicals, lipid peroxidation and DNA damage Marnett, Lawrence J. Toxicology, Vol. 181-182 https://doi.org/10.1016/S0300-483X(02)00448-1	journal	December 2002
The conceptual design of a hybrid life support system based on the evaluation and comparison of terrestrial testbeds Czupalla, M.; Horneck, G.; Blome, H. J. Advances in Space Research, Vol. 35, Issue 9 https://doi.org/10.1016/j.asr.2005.06.010	journal	January 2005
The neuronal class 2 TSR proteins F-spondin and Mindin: a small family with divergent biological activities Feinstein, Yael; Klar, Avihu The International Journal of Biochemistry & Cell Biology, Vol. 36, Issue 6 https://doi.org/10.1016/j.biocel.2004.01.002	journal	June 2004
Cardiac Period 2 in myocardial ischemia: Clinical implications of a light dependent protein Bonney, Stephanie; Hughes, Kelly; Harter, Patrick N. The International Journal of Biochemistry & Cell Biology, Vol. 45, Issue 3 https://doi.org/10.1016/j.biocel.2012.12.022	journal	March 2013
Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors Takahashi, Kazutoshi; Yamanaka, Shinya Cell, Vol. 126, Issue 4 https://doi.org/10.1016/j.cell.2006.07.024	journal	August 2006
PER2 Controls Lipid Metabolism by Direct Regulation of PPARγ Grimaldi, Benedetto; Bellet, Marina Maria; Katada, Sayako Cell Metabolism, Vol. 12, Issue 5 https://doi.org/10.1016/j.cmet.2010.10.005	journal	November 2010
(Re)inventing the Circadian Feedback Loop Brown, Steven A.; Kowalska, Elzbieta; Dallmann, Robert Developmental Cell, Vol. 22, Issue 3 https://doi.org/10.1016/j.devcel.2012.02.007	journal	March 2012
Dynamics of TGF-β/Smad signaling Zi, Zhike; Chapnick, Douglas A.; Liu, Xuedong FEBS Letters, Vol. 586, Issue 14 https://doi.org/10.1016/j.febslet.2012.03.063	journal	April 2012
Tcap gene mutations in hypertrophic cardiomyopathy and dilated cardiomyopathy Hayashi, Takeharu; Arimura, Takuro; Itoh-Satoh, Manatsu Journal of the American College of Cardiology, Vol. 44, Issue 11 https://doi.org/10.1016/j.jacc.2004.08.058	journal	December 2004
Galactic cosmic ray simulation at the NASA Space Radiation Laboratory Norbury, John W.; Schimmerling, Walter; Slaba, Tony C. Life Sciences in Space Research, Vol. 8 https://doi.org/10.1016/j.lssr.2016.02.001	journal	February 2016
Impact of Circadian Disruption on Cardiovascular Function and Disease Chellappa, Sarah L.; Vujovic, Nina; Williams, Jonathan S. Trends in Endocrinology & Metabolism, Vol. 30, Issue 10 https://doi.org/10.1016/j.tem.2019.07.008	journal	October 2019
Characteristic of the radiation field in low earth orbit and in deep space Reitz, Guenther Zeitschrift für Medizinische Physik, Vol. 18, Issue 4 https://doi.org/10.1016/j.zemedi.2008.06.015	journal	December 2008
Androgen receptor: structure, role in prostate cancer and drug discovery Tan, MH Eileen; Li, Jun; Xu, H. Eric Acta Pharmacologica Sinica, Vol. 36, Issue 1 https://doi.org/10.1038/aps.2014.18	journal	June 2014
The P2X7 receptor is a key modulator of aerobic glycolysis Amoroso, F.; Falzoni, S.; Adinolfi, E. Cell Death & Disease, Vol. 3, Issue 8 https://doi.org/10.1038/cddis.2012.105	journal	August 2012
Regulation of B-1a cells: another novel function of the basic helix-loop-helix transcriptional regulator BHLHE41 Samten, Buka Cellular & Molecular Immunology, Vol. 14, Issue 10 https://doi.org/10.1038/cmi.2017.75	journal	September 2017
Circadian rhythms govern cardiac repolarization and arrhythmogenesis Jeyaraj, Darwin; Haldar, Saptarsi M.; Wan, Xiaoping Nature, Vol. 483, Issue 7387 https://doi.org/10.1038/nature10852	journal	February 2012
Sall4 modulates embryonic stem cell pluripotency and early embryonic development by the transcriptional regulation of Pou5f1 Zhang, Jinqiu; Tam, Wai-Leong; Tong, Guo Qing Nature Cell Biology, Vol. 8, Issue 10 https://doi.org/10.1038/ncb1481	journal	September 2006
Adora2b-elicited Per2 stabilization promotes a HIF-dependent metabolic switch crucial for myocardial adaptation to ischemia Eckle, Tobias; Hartmann, Katherine; Bonney, Stephanie Nature Medicine, Vol. 18, Issue 5 https://doi.org/10.1038/nm.2728	journal	April 2012
Sonic hedgehog myocardial gene therapy: tissue repair through transient reconstitution of embryonic signaling Kusano, Kengo F.; Pola, Roberto; Murayama, Toshinori Nature Medicine, Vol. 11, Issue 11 https://doi.org/10.1038/nm1313	journal	October 2005
Circadian misalignment affects sleep and medication use before and during spaceflight Flynn-Evans, Erin E.; Barger, Laura K.; Kubey, Alan A. npj Microgravity, Vol. 2, Issue 1 https://doi.org/10.1038/npjmgrav.2015.19	journal	January 2016
TGFβ signalling in context Massagué, Joan Nature Reviews Molecular Cell Biology, Vol. 13, Issue 10 https://doi.org/10.1038/nrm3434	journal	September 2012
Oct4 is a critical regulator of stemness in head and neck squamous carcinoma cells Koo, B. S.; Lee, S. H.; Kim, J. M. Oncogene, Vol. 34, Issue 18 https://doi.org/10.1038/onc.2014.174	journal	June 2014
Circadian regulator NR1D2 regulates glioblastoma cell proliferation and motility Yu, Min; Li, Wenjing; Wang, Qianqian Oncogene, Vol. 37, Issue 35 https://doi.org/10.1038/s41388-018-0319-8	journal	May 2018
CDX2 inhibits the proliferation and tumor formation of colon cancer cells by suppressing Wnt/β-catenin signaling via transactivation of GSK-3β and Axin2 expression Yu, Junhui; Liu, Dong; Sun, Xuejun Cell Death & Disease, Vol. 10, Issue 1 https://doi.org/10.1038/s41419-018-1263-9	journal	January 2019
Aberrant CDKN1A transcriptional response associates with abnormal sensitivity to radiation treatment Badie, C.; Dziwura, S.; Raffy, C. British Journal of Cancer, Vol. 98, Issue 11 https://doi.org/10.1038/sj.bjc.6604381	journal	May 2008
Purification and characterization of a recombinant human Theta-class glutathione transferase (GSTT2-2) Tan, Kian-Leong; Board, Philip G. Biochemical Journal, Vol. 315, Issue 3 https://doi.org/10.1042/bj3150727	journal	May 1996
Molecular mechanisms involved in the control of glycogenosis in skeletal muscle by calcium ions and cyclic AMP Cohen, Philip Biochemical Society Transactions, Vol. 15, Issue 5 https://doi.org/10.1042/bst0150999	journal	October 1987
CCAAT/enhancer-binding protein is required for mitotic clonal expansion during adipogenesis Tang, Q. -Q.; Otto, T. C.; Lane, M. D. Proceedings of the National Academy of Sciences, Vol. 100, Issue 3 https://doi.org/10.1073/pnas.0337434100	journal	January 2003
TNF-TNFR2/p75 signaling inhibits early and increases delayed nontargeted effects in bone marrow-derived endothelial progenitor cells. Sasi, Sharath P.; Song, Jin; Park, Daniel Journal of Biological Chemistry, Vol. 290, Issue 45 https://doi.org/10.1074/jbc.A114.567743	journal	November 2015
Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: a phase I trial Arai, S.; Meagher, R.; Swearingen, M. Cytotherapy, Vol. 10, Issue 6 https://doi.org/10.1080/14653240802301872	journal	January 2008
False discovery rate, sensitivity and sample size for microarray studies Pawitan, Y.; Michiels, S.; Koscielny, S. Bioinformatics, Vol. 21, Issue 13 https://doi.org/10.1093/bioinformatics/bti448	journal	April 2005
Quick calculation for sample size while controlling false discovery rate with application to microarray analysis Liu, Peng; Hwang, J. T. Gene Bioinformatics, Vol. 23, Issue 6 https://doi.org/10.1093/bioinformatics/btl664	journal	January 2007
The sva package for removing batch effects and other unwanted variation in high-throughput experiments Leek, Jeffrey T.; Johnson, W. Evan; Parker, Hilary S. Bioinformatics, Vol. 28, Issue 6 https://doi.org/10.1093/bioinformatics/bts034	journal	January 2012
oposSOM: R-package for high-dimensional portraying of genome-wide expression landscapes on bioconductor: Fig. 1. Löffler-Wirth, Henry; Kalcher, Martin; Binder, Hans Bioinformatics, Vol. 31, Issue 19 https://doi.org/10.1093/bioinformatics/btv342	journal	June 2015
Cardiac-specific mindin overexpression attenuates cardiac hypertrophy via blocking AKT/GSK3β and TGF-β1–Smad signalling Yan, Ling; Wei, Xiang; Tang, Qi-Zhu Cardiovascular Research, Vol. 92, Issue 1 https://doi.org/10.1093/cvr/cvr159	journal	June 2011
The DBP gene is expressed according to a circadian rhythm in the suprachiasmatic nucleus and influences circadian behavior Lopez-Molina, L. The EMBO Journal, Vol. 16, Issue 22 https://doi.org/10.1093/emboj/16.22.6762	journal	November 1997
Rapid detection of octamer binding proteins with ‘mini extracts’, prepared from a small number of cells Schreiber, Edgar; Matthias, Patrick; Müller, Michael M. Nucleic Acids Research, Vol. 17, Issue 15 https://doi.org/10.1093/nar/17.15.6419	journal	January 1989
limma powers differential expression analyses for RNA-sequencing and microarray studies Ritchie, Matthew E.; Phipson, Belinda; Wu, Di Nucleic Acids Research, Vol. 43, Issue 7 https://doi.org/10.1093/nar/gkv007	journal	January 2015
Enrichr: a comprehensive gene set enrichment analysis web server 2016 update Kuleshov, Maxim V.; Jones, Matthew R.; Rouillard, Andrew D. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw377	journal	May 2016
Ecstasy (MDMA) Alters Cardiac Gene Expression and DNA Methylation: Implications for Circadian Rhythm Dysfunction in the Heart Koczor, Christopher A.; Ludlow, Ivan; Hight, Robert S. Toxicological Sciences, Vol. 148, Issue 1 https://doi.org/10.1093/toxsci/kfv170	journal	August 2015
Long noncoding RNA FLRL2 alleviated nonalcoholic fatty liver disease through Arntl‐Sirt1 pathway Chen, Yi; Chen, Xueyang; Gao, Jianguo The FASEB Journal, Vol. 33, Issue 10 https://doi.org/10.1096/fj.201900643RRR	journal	July 2019
A comprehensive analysis of phase I and phase II metabolism gene polymorphisms and risk of colorectal cancer Landi, Stefano; Gemignani, Federica; Moreno, Victor Pharmacogenetics and Genomics, Vol. 15, Issue 8 https://doi.org/10.1097/01.fpc.0000165904.48994.3d	journal	January 2005
TGF-β Signaling from Receptors to Smads Hata, Akiko; Chen, Ye-Guang Cold Spring Harbor Perspectives in Biology, Vol. 8, Issue 9 https://doi.org/10.1101/cshperspect.a022061	journal	July 2016
CLOCK:BMAL1 is a pioneer-like transcription factor Menet, J. S.; Pescatore, S.; Rosbash, M. Genes & Development, Vol. 28, Issue 1 https://doi.org/10.1101/gad.228536.113	journal	January 2014
Clock genes alterations and endocrine disorders Angelousi, Anna; Kassi, Eva; Nasiri-Ansari, Narjes European Journal of Clinical Investigation, Vol. 48, Issue 6 https://doi.org/10.1111/eci.12927	journal	April 2018
Adelmidrol, a palmitoylethanolamide analogue, reduces chronic inflammation in a carrageenin-granuloma model in rats De Filippis, Daniele; D’Amico, Alessandra; Cinelli, Maria Pia Journal of Cellular and Molecular Medicine, Vol. 13, Issue 6 https://doi.org/10.1111/j.1582-4934.2008.00353.x	journal	June 2009
Regulation of the Mechanism of TWIST1 Transcription by BHLHE40 and BHLHE41 in Cancer Cells Asanoma, Kazuo; Liu, Ge; Yamane, Takako Molecular and Cellular Biology, Vol. 35, Issue 24 https://doi.org/10.1128/MCB.00678-15	journal	December 2015
Low-dose radiation affects cardiac physiology: gene networks and molecular signaling in cardiomyocytes Coleman, Matthew A.; Sasi, Sharath P.; Onufrak, Jillian American Journal of Physiology-Heart and Circulatory Physiology, Vol. 309, Issue 11 https://doi.org/10.1152/ajpheart.00050.2015	journal	December 2015
Particle Radiation-Induced Nontargeted Effects in Bone-Marrow-Derived Endothelial Progenitor Cells Sasi, Sharath P.; Park, Daniel; Muralidharan, Sujatha Stem Cells International, Vol. 2015 https://doi.org/10.1155/2015/496512	journal	January 2015
PIK3IP1, a Negative Regulator of PI3K, Suppresses the Development of Hepatocellular Carcinoma He, Xin; Zhu, Zhenqi; Johnson, Carla Cancer Research, Vol. 68, Issue 14 https://doi.org/10.1158/0008-5472.CAN-08-0025	journal	July 2008
CDX2 Regulates Multidrug Resistance 1 Gene Expression in Malignant Intestinal Epithelium Takakura, Y.; Hinoi, T.; Oue, N. Cancer Research, Vol. 70, Issue 17 https://doi.org/10.1158/0008-5472.CAN-09-4701	journal	August 2010
Pik3ip1 Is a Negative Immune Regulator that Inhibits Antitumor T cell Immunity Chen, Yichen; Wang, Jun; Wang, Xi Clinical Cancer Research https://doi.org/10.1158/1078-0432.CCR-18-4134	journal	July 2019
TCF21: Flipping the Phenotypic Switch in SMC Xie, Yi; Martin, Kathleen A. Circulation Research, Vol. 126, Issue 4 https://doi.org/10.1161/CIRCRESAHA.120.316533	journal	February 2020
Increased Vascular Senescence and Impaired Endothelial Progenitor Cell Function Mediated by Mutation of Circadian Gene Per2 Wang, Chao-Yung; Wen, Ming-Shien; Wang, Hong-Wei Circulation, Vol. 118, Issue 21 https://doi.org/10.1161/CIRCULATIONAHA.108.790469	journal	November 2008
The extracellular matrix protein mindin serves as an integrin ligand and is critical for inflammatory cell recruitment Jia, Wei; Li, Hong; He, You-Wen Blood, Vol. 106, Issue 12 https://doi.org/10.1182/blood-2005-04-1658	journal	December 2005
Enhanced susceptibility of cyclin kinase inhibitor p21 knockout mice to high fat diet induced atherosclerosis Khanna, Ashwani K. Journal of Biomedical Science, Vol. 16, Issue 1 https://doi.org/10.1186/1423-0127-16-66	journal	January 2009
Expression cartography of human tissues using self organizing maps Wirth, Henry; Löffler, Markus; von Bergen, Martin BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-306	journal	July 2011
Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool Chen, Edward Y.; Tan, Christopher M.; Kou, Yan BMC Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2105-14-128	journal	January 2013
Risk-conscious correction of batch effects: maximising information extraction from high-throughput genomic datasets Oytam, Yalchin; Sobhanmanesh, Fariborz; Duesing, Konsta BMC Bioinformatics, Vol. 17, Issue 1 https://doi.org/10.1186/s12859-016-1212-5	journal	September 2016
Genomics of circadian rhythms in health and disease Rijo-Ferreira, Filipa; Takahashi, Joseph S. Genome Medicine, Vol. 11, Issue 1 https://doi.org/10.1186/s13073-019-0704-0	journal	December 2019
Ceramide- and ERK-dependent pathway for the activation of CCAAT/enhancer binding protein by interleukin-1β in hepatocytes Giltiay, Natalia V.; Karakashian, Alexander A.; Alimov, Alexander P. Journal of Lipid Research, Vol. 46, Issue 11 https://doi.org/10.1194/jlr.M500337-JLR200	journal	November 2005
Circadian clock-mediated control of stem cell division and differentiation: beyond night and day Brown, Steven A. Development, Vol. 141, Issue 16 https://doi.org/10.1242/dev.104851	journal	August 2014
Harderian Gland Tumorigenesis: Low-Dose and LET Response Chang, Polly Y.; Cucinotta, Francis A.; Bjornstad, Kathleen A. Radiation Research, Vol. 185, Issue 5 https://doi.org/10.1667/RR14335.1	journal	May 2016
Divergent Modification of Low-Dose 56Fe-Particle and Proton Radiation on Skeletal Muscle Shtifman, Alexander; Pezone, Matthew J.; Sasi, Sharath P. Radiation Research, Vol. 180, Issue 5 https://doi.org/10.1667/RR3329.1	journal	October 2013
SALL4 activates TGF-β/SMAD signaling pathway to induce EMT and promote gastric cancer metastasis Zhang, Xu; Zhang, Peng; Shao, Meng Cancer Management and Research, Vol. Volume 10 https://doi.org/10.2147/CMAR.S177373	journal	January 2018
p21--Negative Regulator of the Cell Cycle Gartel, A. L.; Serfas, M. S.; Tyner, A. L. Experimental Biology and Medicine, Vol. 213, Issue 2 https://doi.org/10.3181/00379727-213-44046	journal	November 1996
Establishment of a Colorectal Cancer-Related MicroRNA-mRNA Regulatory Network by Microarray and Bioinformatics Jiang, Dan; Xie, Xiaoliang; Lu, Zhenhui Frontiers in Genetics, Vol. 11 https://doi.org/10.3389/fgene.2020.560186	journal	October 2020
P2X7 on Mouse T Cells: One Channel, Many Functions Rissiek, BjÃ¶rn; Haag, Friedrich; Boyer, Olivier Frontiers in Immunology, Vol. 6 https://doi.org/10.3389/fimmu.2015.00204	journal	May 2015
Human Pathophysiological Adaptations to the Space Environment Demontis, Gian C.; Germani, Marco M.; Caiani, Enrico G. Frontiers in Physiology, Vol. 8 https://doi.org/10.3389/fphys.2017.00547	journal	August 2017
Time-Dependent miRNA Profile during Septic Acute Kidney Injury in Mice Tod, Pál; Róka, Beáta; Kaucsár, Tamás International Journal of Molecular Sciences, Vol. 21, Issue 15 https://doi.org/10.3390/ijms21155316	journal	July 2020
Epigenetic silencing of ARNTL, a circadian gene and potential tumor suppressor in ovarian cancer Yeh, Chia-Ming; Shay, Jacqueline; Zeng, Ting-Chuan International Journal of Oncology, Vol. 45, Issue 5 https://doi.org/10.3892/ijo.2014.2627	journal	August 2014
Effect of STC2 gene silencing on colorectal cancer cells Li, Qianyuan; Zhou, Xiukou; Fang, Zhengyu Molecular Medicine Reports https://doi.org/10.3892/mmr.2019.10332	journal	June 2019
The peroxisome proliferator-activated receptor: A family of nuclear receptors role in various diseases Tyagi, Sandeep; Sharma, Saurabh; Gupta, Paras Journal of Advanced Pharmaceutical Technology & Research, Vol. 2, Issue 4 https://doi.org/10.4103/2231-4040.90879	journal	January 2011
MiR-589-5p is a potential prognostic marker of hepatocellular carcinoma and regulates tumor cell growth by targeting MIG-6 Xu, M.; Wang, Y.; He, H. T. Neoplasma, Vol. 65, Issue 05 https://doi.org/10.4149/neo_2018_171125N762	journal	January 2018
Risk-conscious correction of batch effects: maximising information extraction from high-throughput genomic datasets Oytam, Yalchin; Sobhanmanesh, Fariborz; Duesing, Konsta Figshare https://doi.org/10.6084/m9.figshare.c.3641393.v1	collection	January 2016

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