Effect of simulated microgravity on metabolism of HGC‑27 gastric cancer cells
- Authors:
- Zheng‑Yang Chen
- Nan Jiang
- Song Guo
- Bin‑Bin Li
- Jia‑Qi Yang
- Shao‑Bin Chai
- Hong‑Feng Yan
- Pei‑Ming Sun
- Tao Zhang
- Hong‑Wei Sun
- He‑Ming Yang
- Jin‑Lian Zhou
- Yan Cui
-
Affiliations: Department of General Surgery, The People's Liberation Army 306th Hospital of Peking University Teaching Hospital, Beijing 100101, P.R. China, Department of General Surgery, The People's Liberation Army 306th Hospital, Beijing 100101, P.R. China, Department of Pathology, The People's Liberation Army 306th Hospital, Beijing 100101, P.R. China - Published online on: March 10, 2020 https://doi.org/10.3892/ol.2020.11451
- Pages: 3439-3450
-
Copyright: © Chen et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Fedotov AA, Akulov SA and Akulova AS: Alterations in cardiovascular system under artificially simulated microgravity: Preliminary study. Conf Proc IEEE Eng Med Biol Soc. 2016:204–206. 2016.PubMed/NCBI | |
Atomi Y: Gravitational Effects on human physiology. Subcell Biochem. 72:627–59. 2015. View Article : Google Scholar : PubMed/NCBI | |
Hughes-Fulford M: Changes in gene expression and signal transduction in microgravity. J Gravit Physiol. 8:P1–4. 2001.PubMed/NCBI | |
Ulbrich C, Wehland M, Pietsch J, Aleshcheva G, Wise P, van Loon J, Magnusson N, Infanger M, Grosse J, Eilles C, et al: The impact of simulated and real microgravity on bone cells and mesenchymal stem cells. Biomed Res Int. 2014:9285072014. View Article : Google Scholar : PubMed/NCBI | |
Riwaldt S, Bauer J, Wehland M, Slumstrup L, Kopp S, Warnke E, Dittrich A, Magnusson NE, Pietsch J, Corydon TJ, et al: Pathways regulating spheroid formation of human follicular thyroid cancer cells under simulated microgravity conditions: A genetic approach. Int J Mol Sci. 17:5282016. View Article : Google Scholar : PubMed/NCBI | |
Svejgaard B, Wehland M, Ma X, Kopp S, Sahana J, Warnke E, Aleshcheva G, Hemmersbach R, Hauslage J, Grosse J, et al: Common effects on cancer cells exerted by a randompositioning machine and a 2D clinostat. PLoS One. 10:e01351572015. View Article : Google Scholar : PubMed/NCBI | |
Sahana J, Nassef MZ, Wehland M, Kopp S, Krüger M, Corydon TJ, Infanger M, Bauer J and Grimm D: Decreased E-cadherin in MCF-7 human breast cancer cells forming multicellular spheroids exposed to simulated microgravity. Proteomics. 18:e18000152018. View Article : Google Scholar : PubMed/NCBI | |
Vidyasekar P, Shyamsunder P, Arun R, Santhakumar R, Kapadia NK, Kumar R and Verma RS: Genome wide expression profiling of cancer cell lines cultured in microgravity reveals significant dysregulation of cell cycle and MicroRNA gene networks. PLoS One. 10:e01359582015. View Article : Google Scholar : PubMed/NCBI | |
Dietz C, Infanger M, Romswinkel A, Strube F and Kraus A: Apoptosis induction and alteration of cell adherence in human lung cancer cells under simulated microgravity. Int J Mol Sci. 20(pii): E36012019. View Article : Google Scholar : PubMed/NCBI | |
Kim YJ, Jeong AJ, Kim M, Lee C, Ye SK and Kim S: Time-averaged simulated microgravity (taSMG) inhibits proliferation of lymphoma cells, L-540 and HDLM-2, using a 3D clinostat. Biomed Eng Online. 16:482017. View Article : Google Scholar : PubMed/NCBI | |
Warburg O: On respiratory impairment in cancer cells. Science. 124:269–272. 1956.PubMed/NCBI | |
Nath S and Villadsen J: Oxidative phosphorylation revisited. Biotechnol Bioeng. 112:429–437. 2015. View Article : Google Scholar : PubMed/NCBI | |
Hanahan D and Weinberg RA: Hallmarks of cancer: The next generation. Cell. 144:646–74. 2011. View Article : Google Scholar : PubMed/NCBI | |
Hu JD, Tang HQ, Zhang Q, Fan J, Hong J, Gu JZ and Chen JL: Prediction of gastric cancer metastasis through urinary metabolomics investigation using GC/MS. World J Gastroenterol. 17:727–734. 2011. View Article : Google Scholar : PubMed/NCBI | |
Chen JL, Tang HQ, Hu JD, Fan J, Hong J and Gu JZ: Metabolomics of gastric cancer metastasis detected by gas chromatography and mass spectrometry. World J Gastroenterol. 16:5874–5880. 2010. View Article : Google Scholar : PubMed/NCBI | |
Gatenby RA and Gillies RJ: Why do cancers have high aerobic glycolysis. Nat Rev Cancer. 4:891–899. 2004. View Article : Google Scholar : PubMed/NCBI | |
Koukourakis MI, Pitiakoudis M, Giatromanolaki A, Tsarouha A, Polychronidis A, Sivridis E and Simopoulos C: Oxygen and glucose consumption in gastrointestinal adenocarcinomas: Correlation with markers of hypoxia, acidity and anaerobic glycolysis. Cancer Sci. 97:1056–1060. 2006. View Article : Google Scholar : PubMed/NCBI | |
Pedersen PL, Mathupala S, Rempel A, Geschwind JF and Ko YH: A key player in the growth and survival of many cancers and an ideal prospect for therapeutic intervention. Biochim Biophys Acta. 1555:14–20. 2002. View Article : Google Scholar : PubMed/NCBI | |
Tech K, Tikunov AP, Farooq H, Morrissy AS, Meidinger J, Fish T, Green SC, Liu H, Li Y, Mungall AJ, et al: Pyruvate kinase inhibits proliferation during postnatal cerebellar neurogenesis and suppresses medulloblastoma formation. Cancer Res. 77:3217–3230. 2017. View Article : Google Scholar : PubMed/NCBI | |
An J, Zhang Y, He J, Zang Z, Zhou Z, Pei X, Zheng X, Zhang W, Yang H and Li S: Lactate dehydrogenase A promotes the invasion and proliferation of pituitary adenoma. Sci Rep. 7:47342017. View Article : Google Scholar : PubMed/NCBI | |
Israelsen WJ and Vander Heiden MG: Pyruvate kinase: Function, regulation and role in cancer. Semin Cell Dev Biol. 43:43–51. 2015. View Article : Google Scholar : PubMed/NCBI | |
Wu J, Hu L, Chen M, Cao W, Chen H and He T: Pyruvate kinase M2 overexpression and poor prognosis in solid tumors of digestive system: Evidence from 16 cohort studies. Onco Targets Ther. 9:4277–4288. 2016. View Article : Google Scholar : PubMed/NCBI | |
Jové M, Collado R, Quiles JL, Ramírez-Tortosa MC, Sol J, Ruiz-Sanjuan M, Fernandez M, de la Torre Cabrera C, Ramírez-Tortosa C, Granados-Principal S, et al: A plasma metabolomic signature discloses human breast cancer. Oncotarget. 8:19522–19533. 2017. View Article : Google Scholar : PubMed/NCBI | |
Pandey R, Caflisch L, Lodi A1, Brenner AJ and Tiziani S: Metabolomic signature of brain cancer. Mol Carcinog. 56:2355–2371. 2017. View Article : Google Scholar : PubMed/NCBI | |
Navas-Carrillo D, Rodriguez JM, Montoro-García S and Orenes-Piñero E: High-resolution proteomics and metabolomics in thyroid cancer: Deciphering novel biomarkers. Crit Rev Clin Lab Sci. 54:446–457. 2017. View Article : Google Scholar : PubMed/NCBI | |
Chen L, Yang X, Cui X, Jiang MM, Gui Y, Zhang YN and Luo XD: Adrenomedullin is a key protein mediating rotary cell culture system that induces the effects of simulated microgravity on human breast cancer Cells. Microgravity Sci Technol. 27:417–426. 2015. View Article : Google Scholar | |
Michaletti A, Gioia M, Tarantino U and Zolla L: Effects of microgravity on osteoblast mitochondria: A proteomic and metabolomics profile. Sci Rep. 7:153762017. View Article : Google Scholar : PubMed/NCBI | |
Morabito C, Steimberg N, Mazzoleni G, Guarnieri S, Fanò-Illic G and Mariggiò MA: RCCS bioreactor-based modelled microgravity induces significant changes on in vitro 3D neuroglial cell cultures. Biomed Res Int. 2015:7542832015. View Article : Google Scholar : PubMed/NCBI | |
Longo N, Frigeni M and Pasquali M: Carnitine transport and fatty acid oxidation. Biochim Biophys Acta. 1863:2422–2435. 2016. View Article : Google Scholar : PubMed/NCBI | |
Pietsch J, Ma X, Wehland M, Aleshcheva G, Schwarzwälder A, Segerer J, Birlem M, Horn A, Bauer J, Infanger M and Grimm D: Spheroid formation of human thyroid cancer cells in an automated culturing system during the Shenzhou-8 Space mission. Biomaterials. 34:7694–705. 2013. View Article : Google Scholar : PubMed/NCBI | |
Riwaldt S, Pietsch J, Sickmann A, Bauer J, Braun M, Segerer J, Schwarzwälder A, Aleshcheva G, Corydon TJ, Infanger M and Grimm D: Identification of proteins involved in inhibition of spheroid formation under microgravity. Proteomics. 15:2945–2952. 2015. View Article : Google Scholar : PubMed/NCBI | |
Arun RP, Sivanesan D, Vidyasekar P and Verma RS: PTEN/FOXO3/AKT pathway regulates cell death and mediates morphogenetic differentiation of Colorectal Cancer Cells under Simulated Microgravity. Sci Rep. 7:59522017. View Article : Google Scholar : PubMed/NCBI | |
Kopp S, Sahana J, Islam T, Petersen AG, Bauer J, Corydon TJ, Schulz H, Saar K, Huebner N, Slumstrup L, et al: The role of NFκB in spheroid formation of human breast cancer cells cultured on the random positioning machine. Sci Rep. 8:9212018. View Article : Google Scholar : PubMed/NCBI | |
Chen ZY, Guo S, Li BB, Jiang N, Li A, Yan HF, Yang HM, Zhou JL, Li CL and Cui Y: Effect of weightlessness on the 3D structure formation and physiologic function of human cancer cells. Biomed Res Int. 2019:48940832019.PubMed/NCBI | |
Marín de Mas I, Aguilar E, Jayaraman A, Polat IH, Martín-Bernabé A, Bharat R, Foguet C, Milà E, Papp B, Centelles JJ and Cascante M: Cancer cell metabolism as new targets for novel designed therapies. Future Med Chem. 6:1791–1810. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zhu M, Jin XW, Wu BY, Nie JL and Li YH: Effects of simulated weightlessness on cellular morphology and biological characteristics of cell lines SGC-7901 and HFE-145. Genet Mol Res. 13:6060–6069. 2014. View Article : Google Scholar : PubMed/NCBI | |
Espinosa-Jeffrey A, Nguyen K, Kumar S, Toshimasa O, Hirose R, Reue K, Vergnes L, Kinchen J and Vellis J: Simulated microgravity enhances oligodendrocyte mitochondrial function and lipid metabolism. J Neurosci Res. 94:1434–1450. 2016. View Article : Google Scholar : PubMed/NCBI | |
Akagi T and Kimoto T: Human cell line (HGC-27) derived from the metastatic lymph node of gastric cancer. Acta Med Okayama. 30:215–219. 1976.PubMed/NCBI | |
Kawakami H, Zaanan A and Sinicrope FA: Microsatellite instability testing and its role in the management of colorectal cancer. Curr Treat Options Oncol. 16:302015. View Article : Google Scholar : PubMed/NCBI | |
Zalba S and Ten Hagen TL: Cell membrane modulation as adjuvant in cancer therapy. Cancer Treat Rev. 52:48–57. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kim HY, Lee KM, Kim SH, Kwon YJ, Chun YJ and Choi HK: Comparative metabolic and lipidomic profiling of human breast cancer cells with different metastatic potentials. Oncotarget. 7:67111–67128. 2016.PubMed/NCBI | |
Elvas F, Stroobants S and Wyffels L: Phosphatidylethanolamine targeting for cell death imaging in early treatment response evaluation and disease diagnosis. Apoptosis. 22:971–987. 2017. View Article : Google Scholar : PubMed/NCBI | |
Iorio E, Ricci A, Bagnoli M, Pisanu ME, Castellano G, Di Vito M, Venturini E, Glunde K, Bhujwalla ZM, Mezzanzanica D, et al: Activation of phosphatidylcholine cycle enzymes in human epithelial ovarian cancer cells. Cancer Res. 70:2126–2135. 2010. View Article : Google Scholar : PubMed/NCBI | |
Grimm D, Bauer J, Kossmehl P, Shakibaei M, Schöberger J, Pickenhahn H, Schulze-Tanzil G, Vetter R, Eilles C, Paul M and Cogoli A: Simulated microgravity alters differentiation and increases apoptosis in human follicular thyroid carcinoma cells. FASEB J. 16:604–606. 2002. View Article : Google Scholar : PubMed/NCBI | |
Kossmehl P, Shakibaei M, Cogoli A, Infanger M, Curcio F, Schönberger J, Eilles C, Bauer J, Pickenhahn H, Schulze-Tanzil G, et al: Weightlessness induced apoptosis in normal thyroid cells and papillary thyroid carcinoma cells via extrinsic and intrinsic pathways. Endocrinology. 144:4172–4179. 2003. View Article : Google Scholar : PubMed/NCBI | |
Masiello MG, Cucina A, Proietti S, Palombo A, Coluccia P, D'Anselmi F, Dinicola S, Pasqualato A, Morini V and Bizzarri M: Phenotypic switch induced by simulated microgravity on MDA-MB-231 breast cancer cells. Biomed Res Int. 2014:6524342014. View Article : Google Scholar : PubMed/NCBI | |
Zhao J, Ma H, Wu L, Cao L, Yang Q, Dong H, Wang Z, Ma J and Li Z: The influence of simulated microgravity on proliferation and apoptosis in U251 glioma cells. In Vitro Cell Dev Biol Anim. 53:744–751. 2017. View Article : Google Scholar : PubMed/NCBI | |
Paulick MG and Bertozzi CR: The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for protein. Biochemistry. 47:6991–7000. 2008. View Article : Google Scholar : PubMed/NCBI | |
Ferguson MA, Homans SW, Dwek RA and Rademacher TW: Glycosyl-phosphatidylinositol moiety that anchors Trypanosoma brucei variant surface glycoprotein to the membrane. Science. 239:753–759. 1988. View Article : Google Scholar : PubMed/NCBI | |
Ferguson MA: The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J Cell Sci. 112:2799–2809. 1999.PubMed/NCBI | |
Tsai YH, Liu X and Seeberger PH: Chemical biology of glycosylphosphatidylinositol anchors. Angew Chem Int Ed Engl. 51:11438–11456. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chang D, Xu H, Guo Y, Jiang X, Liu Y, Li K, Pan C, Yuan M, Wang J, Li T and Liu C: Simulated microgravity alters the metastatic potential of a human lung adenocarcinoma cell line. In Vitro Cell Dev Biol Anim. 49:170–177. 2019. View Article : Google Scholar | |
Qian A, Zhang W, Xie L, Weng Y, Yang P, Wang Z, Hu L, Xu HY, Tian ZC and Shang P: Simulated weightlessness alters biological characteristics of human breast cancer cell line MCF-7. Acta Astronautica. 63:947–958. 2008. View Article : Google Scholar | |
Peng W, Tan S, Xu Y, Wang L, Qiu D, Cheng C, Lin Y, Liu C, Li Z, Li Y, et al: LC-MS/MS metabolome analysis detects the changes in the lipid metabolic profiles of dMMR and pMMR cells. Oncol Rep. 40:1026–1034. 2018.PubMed/NCBI | |
Toshima K, Nagafuku M, Okazaki T, Kobayashi T and Inokuchi JI: Plasma membrane sphingomyelin modulates thymocyte development by inhibiting TCR-induced apoptosis. Int Immunol. 31:211–223. 2019. View Article : Google Scholar : PubMed/NCBI | |
Hogan PG: Sphingomyelin, ORAI1 channels, and cellular Ca2+ signaling. J Gen Physiol. 146:195–200. 2015. View Article : Google Scholar : PubMed/NCBI | |
Matanes F, Twal WO and Hammad SM: Sphingolipids as biomarkers of disease. Adv Exp Med Biol. 1159:109–138. 2019. View Article : Google Scholar : PubMed/NCBI | |
Kohama T, Olivera A, Edsall L, Nagiec MM, Dickson R and Spiegel S: Molecular cloning and functional characterization of murine sphingosine kinase. J Biol Chem. 273:23722–23728. 1998. View Article : Google Scholar : PubMed/NCBI | |
Li J, Gray BD, Pak KY and Ng CK: Targeting phosphatidylethanolamine and phosphatidylserine for imaging apoptosis in cancer. Nucl Med Biol. 78:23–30. 2019. View Article : Google Scholar : PubMed/NCBI | |
Andrieu-Abadie N and Levade T: Sphingomyelin hydrolysis during apoptosis. Biochim Biophys Acta. 1585:126–134. 2002. View Article : Google Scholar : PubMed/NCBI | |
van der Hoeven D, Cho KJ, Zhou Y, Ma X, Chen W, Naji A, Montufar-Solis D, Zuo Y, Kovar SE, Levental KR, et al: Sphingomyelin metabolism is a regulator of K-Ras function. Mol Cell Biol. 38(pii): e00373–17. 2018.PubMed/NCBI | |
Fernández-Medarde A and Santos E: Ras in cancer and developmental diseases. Genes Cancer. 2:344–358. 2011. View Article : Google Scholar : PubMed/NCBI | |
Cacev T, Radosević S, Spaventi R, Pavelić K and Kapitanović S: NF1 gene loss of heterozygosity and expression analysis in sporadic colon cancer. Gut. 54:1129–1135. 2005. View Article : Google Scholar : PubMed/NCBI | |
Dhomen N and Marais R: New insight into BRAF mutations in cancer. Curr Opin Genet Dev. 17:31–39. 2007. View Article : Google Scholar : PubMed/NCBI | |
Khoukaz T: Administration of anti-EGFR therapy: A practical review. Semin Oncol Nurs. 22:20–27. 2006. View Article : Google Scholar : PubMed/NCBI | |
Baek MO, Ahn CB, Cho HJ, Choi JY, Son KH and Yoon MS: Simulated microgravity inhibits C2C12 myogenesis via phospholipase D2-induced Akt/FOXO1 regulation. Sci Rep. 9:149102019. View Article : Google Scholar : PubMed/NCBI | |
Wang Z, Zhang F, He J, Wu P, Tay LWR, Cai M, Nian W, Weng Y, Qin L, Chang JT, et al: Binding of PLD2-generated phosphatidic acid to KIF5B promotes MT1-MMP surface trafficking and lung metastasis of mouse breast cancer cells. Dev Cell. 43:186–197. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zeiller C, Mebarek S, Jaafar R, Pirola L, Lagarde M, Prigent AF and Némoz G: Phospholipase D2 regulates endothelial permeability through cytoskeleton reorganization and occludin downregulation. Biochim Biophys Acta. 1793:1236–1249. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ngo Thai Bich V, Hongu T, Miura Y, Katagiri N, Ohbayashi N, Yamashita-Kanemaru Y, Shibuya A, Funakoshi Y and Kanaho Y: Physiological function of phospholipase D2 in anti-tumor immunity: Regulation of CD8+ T lymphocyte proliferation. Sci Rep. 8:62832018. View Article : Google Scholar : PubMed/NCBI | |
Kandori S, Kojima T, Matsuoka T, Yoshino T, Sugiyama A, Nakamura E, Shimazui T, Funakoshi Y, Kanaho Y and Nishiyama H: Phospholipase D2 promotes disease progression of renal cell carcinoma through the induction of angiogenin. Cancer Sci. 109:1865–1875. 2018. View Article : Google Scholar : PubMed/NCBI | |
Guo L, Cui C, Zhang K, Wang J, Wang Y, Lu Y, Chen K, Yuan J, Xiao G, Tang B, et al: Kindlin-2 links mechano-environment to proline synthesis and tumor growth. Nat Commun. 10:8452019. View Article : Google Scholar : PubMed/NCBI | |
Phang JM, Donald SP, Pandhare J and Liu Y: The metabolism of proline, a stress substrate, modulates carcinogenic pathways. Amino Acids. 35:681–690. 2008. View Article : Google Scholar : PubMed/NCBI | |
Liu W, Wang X, Liu Z, Wang Y, Yin B, Yu P, Duan X, Liao Z, Chen Y, Liu C, et al: SGK1 inhibition induces autophagy-dependent apoptosis via the mTOR-Foxo3a pathway. Br J Cancer. 117:1139–1153. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wallimann T, Tokarska-Schlattner M and Schlattner U: The creatine kinase system and pleiotropic effects of creatine. Amino Acids. 40:1271–1296. 2011. View Article : Google Scholar : PubMed/NCBI | |
Campos-Ferraz PL, Gualano B, das Neves W, Andrade IT, Hangai I, Pereira RT, Bezerra RN, Deminice R, Seelaender M and Lancha AH: Exploratory studies of the potential anti-cancer effects of creatine. Amino Acids. 48:1993–2001. 2016. View Article : Google Scholar : PubMed/NCBI | |
Martin KJ, Chen SF, Clark GM, Degen D, Wajima M, Von Hoff DD and Kaddurah-Daouk R: Evaluation of creatine analogs as a new class of anticancer agents using freshly explanted human tumor cells. J Natl Cancer Inst. 86:608–613. 1994. View Article : Google Scholar : PubMed/NCBI | |
Miller EE, Evans AE and Cohn M: Inhibition of rate of tumor growth by creatine and cyclocreatine. Proc Natl Acad Sci USA. 90:3304–3308. 1993. View Article : Google Scholar : PubMed/NCBI | |
Hoppeler H and Fluck M: Plasticity of skeletal muscle mitochondria: Structure and function. Med Sci Sports Exerc. 35:95–104. 2003. View Article : Google Scholar : PubMed/NCBI | |
Adams SH, Hoppel CL, Lok KH, Zhao L, Wong SW, Minkler PE, Hwang DH, Newman JW and Garvey WT: Plasma acylcarnitine profiles suggest incomplete long-chain fatty acid beta-oxidation and altered tricarboxylic acid cycle activity in type 2 diabetic African-American women. J Nutr. 139:1073–1081. 2009. View Article : Google Scholar : PubMed/NCBI | |
Chen WW, Freinkman E, Wang T, Birsoy K and Sabatini DM: Absolute quantification of matrix metabolites reveals the dynamics of mitochondrial metabolism. Cell. 166:1324–1337. 2016. View Article : Google Scholar : PubMed/NCBI | |
Hutschenreuther A, Birkenmeier G, Bigl M, Krohn K and Birkemeyer C: Glycerophosphoglycerol, Beta-alanine, and pantothenic acid as metabolic companions of glycolytic activity and cell migration in breast cancer cell lines. Metabolites. 3:1084–1101. 2013. View Article : Google Scholar : PubMed/NCBI | |
Leonardi R and Jackowski S: Biosynthesis of pantothenic acid and coenzyme A. EcoSal Plus. 2:2007. View Article : Google Scholar : PubMed/NCBI | |
Vurusaner B, Poli G and Basaga H: Tumor suppressor genes and ROS: Complex networks of interactions. Free Radic Biol Med. 52:7–18. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gomes AR, Brosens JJ and Lam EW: Resist or die: FOXO transcription factors determine the cellular response to chemotherapy. Cell Cycle. 7:3133–3136. 2008. View Article : Google Scholar : PubMed/NCBI | |
Hou YQ, Yao Y, Bao YL, Song ZB, Yang C, Gao XL, Zhang WJ, Sun LG, Yu CL, Huang YX, et al: Juglanthraquinone C induces intracellular ROS increase and apoptosis by activating the Akt/Foxo signal pathway in HCC cells. Oxid Med Cell Longev. 2016:49416232016. View Article : Google Scholar : PubMed/NCBI | |
Maiese K, Chong ZZ, Hou J and Shang YC: Erythropoietin and oxidative stress. Curr Neurovasc Res. 5:125–142. 2008. View Article : Google Scholar : PubMed/NCBI | |
Nakamura T and Sakamoto K: Forkhead transcription factor FOXO subfamily is essential for reactive oxygen species-induced apoptosis. Mol Cell Endocrinol. 281:47–55. 2008. View Article : Google Scholar : PubMed/NCBI | |
Barthélémy C, Henderson CE and Pettmann B: Foxo3a induces motoneuron death through the Fas pathway in cooperation with JNK. BMC Neurosci. 5(48)2004. | |
Maiese K, Chong ZZ, Li F and Shang YC: Erythropoietin: Elucidating new cellular targets that broaden therapeutic strategies. Prog Neurobiol. 85:194–213. 2008. View Article : Google Scholar : PubMed/NCBI | |
Nowak K, Killmer K, Gessner C and Lutz W: E2F-1 regulates expression of FOXO1 and FOXO3a. Biochim Biophys Acta. 1769:244–252. 2007. View Article : Google Scholar : PubMed/NCBI | |
Liu Y, Ao X, Ding W, Ponnusamy M, Wu W, Hao X, Yu W, Wang Y, Li P and Wang J: Critical role of FOXO3a in carcinogenesis. Mol Cancer. 17:1042018. View Article : Google Scholar : PubMed/NCBI |