Current Drug Targets

Author(s): Wanqian Song, Qiuju Zhang, Zhiyong Cao, Guo Jing, Tiancheng Zhan, Yongkang Yuan, Ning Kang* and Qiang Zhang*

DOI: 10.2174/0113894501325497240918042654

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Targeting SERCA2 in Anti-Tumor Drug Discovery

Page: [1 - 16] Pages: 16

  • * (Excluding Mailing and Handling)

Abstract

SERCA2, a P-type ATPase located on the endoplasmic reticulum of cells, plays an important role in maintaining calcium balance within cells by transporting calcium from the cytoplasm to the endoplasmic reticulum against its concentration gradient. A multitude of studies have demonstrated that the expression of SERCA2 is abnormal in a wide variety of tumor cells. Consequently, research exploring compounds that target SERCA2 may offer a promising avenue for the development of novel anti-tumor drugs. This review has summarized the anti-tumor compounds targeting SERCA2, including thapsigargin, dihydroartemisinin, curcumin, galangin, etc. These compounds interact with SERCA2 on the endoplasmic reticulum membrane, disrupting intracellular calcium ion homeostasis, leading to tumor cell apoptosis, autophagy and cell cycle arrest, ultimately producing anti-tumor effects. Additionally, several potential research directions for compounds targeting SERCA2 as clinical anti-cancer drugs have been proposed in the review. In summary, SERCA2 is a promising anti-tumor target for drug discovery and development.

Keywords: Sarcoplasmic reticulum/endoplasmic reticulum calcium ATPase, cell apoptosis, calcium ion, endoplasmic reticulum stress, autophagy, cell cycle arrest.

Graphical Abstract

[1]
Torre LA, Siegel RL, Ward EM, Jemal A. Global cancer incidence and mortality rates and trends — An update. Cancer Epidemiol Biomarkers Prev 2016; 25(1): 16-27.
[http://dx.doi.org/10.1158/1055-9965.EPI-15-0578] [PMID: 26667886]
[2]
Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021; 71(3): 209-49.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[3]
Wu C, Li M, Meng H, et al. Analysis of status and countermeasures of cancer incidence and mortality in China. Sci China Life Sci 2019; 62(5): 640-7.
[http://dx.doi.org/10.1007/s11427-018-9461-5] [PMID: 30900169]
[4]
Cohen JB, Brown NJ, Brown SA, et al. Cancer therapy–related hypertension: A scientific statement from the american heart association. Hypertension 2023; 80(3): e46-57.
[http://dx.doi.org/10.1161/HYP.0000000000000224] [PMID: 36621810]
[5]
Shyam Sunder S, Sharma UC, Pokharel S. Adverse effects of tyrosine kinase inhibitors in cancer therapy: pathophysiology, mechanisms and clinical management. Signal Transduct Target Ther 2023; 8(1): 262.
[http://dx.doi.org/10.1038/s41392-023-01469-6] [PMID: 37414756]
[6]
Pranzini E, Pardella E, Muccillo L, et al. SHMT2-mediated mitochondrial serine metabolism drives 5-FU resistance by fueling nucleotide biosynthesis. Cell Rep 2022; 40(7): 111233.
[http://dx.doi.org/10.1016/j.celrep.2022.111233] [PMID: 35977477]
[7]
Chambers PJ, Juracic ES, Fajardo VA, Tupling AR. Role of SERCA and sarcolipin in adaptive muscle remodeling. Am J Physiol Cell Physiol 2022; 322(3): C382-94.
[http://dx.doi.org/10.1152/ajpcell.00198.2021] [PMID: 35044855]
[8]
Rodriguez JBR, Muzi-Filho H, Valverde RHF, et al. Rat vas deferens SERCA2 is modulated by Ca2+/calmodulin protein kinase II-mediated phosphorylation. Braz J Med Biol Res 2013; 46(3): 227-34.
[http://dx.doi.org/10.1590/1414-431X20122616] [PMID: 23558856]
[9]
Gorski PA, Ceholski DK, Young HS. Structure-function relationship of the SERCA pump and its regulation by phospholamban and sarcolipin. Adv Exp Med Biol 2017; 981: 77-119.
[http://dx.doi.org/10.1007/978-3-319-55858-5_5] [PMID: 29594859]
[10]
Arbabian A, Brouland JP, Gélébart P, et al. Endoplasmic reticulum calcium pumps and cancer. Biofactors 2011; 37(3): 139-49.
[http://dx.doi.org/10.1002/biof.142] [PMID: 21674635]
[11]
Fan M, Gao J, Zhou L, et al. Highly expressed SERCA2 triggers tumor cell autophagy and is a druggable vulnerability in triple-negative breast cancer. Acta Pharm Sin B 2022; 12(12): 4407-23.
[http://dx.doi.org/10.1016/j.apsb.2022.05.009] [PMID: 36561988]
[12]
Sehgal P, Szalai P, Olesen C, et al. Inhibition of the sarco/endoplasmic reticulum (ER) Ca2+-ATPase by thapsigargin analogs induces cell death via ER Ca2+ depletion and the unfolded protein response. J Biol Chem 2017; 292(48): 19656-73.
[http://dx.doi.org/10.1074/jbc.M117.796920] [PMID: 28972171]
[13]
Mahalingam D, Wilding G, Denmeade S, et al. Mipsagargin, a novel thapsigargin-based PSMA-activated prodrug: Results of a first-in-man phase I clinical trial in patients with refractory, advanced or metastatic solid tumours. Br J Cancer 2016; 114(9): 986-94.
[http://dx.doi.org/10.1038/bjc.2016.72] [PMID: 27115568]
[14]
Zhang Y, Inaba K. Structural basis of the conformational and functional regulation of human SERCA2b, the ubiquitous endoplasmic reticulum calcium pump. BioEssays 2022; 44(7): 2200052.
[http://dx.doi.org/10.1002/bies.202200052] [PMID: 35560336]
[15]
Møller JV, Olesen C, Winther AML, Nissen P. The sarcoplasmic Ca2+ -ATPase: Design of a perfect chemi-osmotic pump. Q Rev Biophys 2010; 43(4): 501-66.
[http://dx.doi.org/10.1017/S003358351000017X] [PMID: 20809990]
[16]
Toyoshima C, Nomura H. Structural changes in the calcium pump accompanying the dissociation of calcium. Nature 2002; 418(6898): 605-11.
[http://dx.doi.org/10.1038/nature00944] [PMID: 12167852]
[17]
Toyoshima C, Mizutani T. Crystal structure of the calcium pump with a bound ATP analogue. Nature 2004; 430(6999): 529-35.
[http://dx.doi.org/10.1038/nature02680] [PMID: 15229613]
[18]
Smolin N, Robia SL. A structural mechanism for calcium transporter headpiece closure. J Phys Chem B 2015; 119(4): 1407-15.
[http://dx.doi.org/10.1021/jp511433v] [PMID: 25531267]
[19]
Britzolaki A, Saurine J, Klocke B, Pitychoutis PM. A role for SERCA Pumps in the neurobiology of neuropsychiatric and neurodegenerative disorders. Adv Exp Med Biol 2020; 1131: 131-61.
[http://dx.doi.org/10.1007/978-3-030-12457-1_6] [PMID: 31646509]
[20]
Musgaard M, Thøgersen L, Schiøtt B. Protonation states of important acidic residues in the central Ca2+ ion binding sites of the Ca2+-ATPase: A molecular modeling study. Biochemistry 2011; 50(51): 11109-20.
[http://dx.doi.org/10.1021/bi201164b] [PMID: 22082179]
[21]
Aguayo-Ortiz R, Espinoza-Fonseca LM. Linking biochemical and structural states of SERCA: Achievements, challenges, and new opportunities. Int J Mol Sci 2020; 21(11): 4146.
[http://dx.doi.org/10.3390/ijms21114146] [PMID: 32532023]
[22]
Toyoshima C, Cornelius F. New crystal structures of PII-type ATPases: Excitement continues. Curr Opin Struct Biol 2013; 23(4): 507-14.
[http://dx.doi.org/10.1016/j.sbi.2013.06.005] [PMID: 23871101]
[23]
Bublitz M, Poulsen H, Morth JP, Nissen P. In and out of the cation pumps: P-Type ATPase structure revisited. Curr Opin Struct Biol 2010; 20(4): 431-9.
[http://dx.doi.org/10.1016/j.sbi.2010.06.007] [PMID: 20634056]
[24]
Andersson J, Hauser K, Karjalainen EL, Barth A. Protonation and hydrogen bonding of Ca2+ site residues in the E2P phosphoenzyme intermediate of sarcoplasmic reticulum Ca2+-ATPase studied by a combination of infrared spectroscopy and electrostatic calculations. Biophys J 2008; 94(2): 600-11.
[http://dx.doi.org/10.1529/biophysj.107.114033] [PMID: 17890386]
[25]
Vangheluwe P, Sepúlveda MR, Missiaen L, Raeymaekers L, Wuytack F, Vanoevelen J. Intracellular Ca2+ - and Mn2+ -Transport ATPases. Chem Rev 2009; 109(10): 4733-59.
[http://dx.doi.org/10.1021/cr900013m] [PMID: 19678701]
[26]
Kekenes-Huskey PM, Metzger VT, Grant BJ, Andrew McCammon J. Calcium binding and allosteric signaling mechanisms for the sarcoplasmic reticulum Ca2+ ATPase. Protein Sci 2012; 21(10): 1429-43.
[http://dx.doi.org/10.1002/pro.2129] [PMID: 22821874]
[27]
Toyoshima C. How Ca2+-ATPase pumps ions across the sarcoplasmic reticulum membrane. Biochim Biophys Acta Mol Cell Res 2009; 1793(6): 941-6.
[http://dx.doi.org/10.1016/j.bbamcr.2008.10.008] [PMID: 19010358]
[28]
Wuytack F, Raeymaekers L, Missiaen L. Molecular physiology of the SERCA and SPCA pumps. Cell Calcium 2002; 32(5-6): 279-305.
[http://dx.doi.org/10.1016/S0143416002001847] [PMID: 12543090]
[29]
Zhihao L, Jingyu N, Lan L, et al. SERCA2a: A key protein in the Ca2+ cycle of the heart failure. Heart Fail Rev 2020; 25(3): 523-35.
[http://dx.doi.org/10.1007/s10741-019-09873-3] [PMID: 31701344]
[30]
Vandecaetsbeek I, Vangheluwe P, Raeymaekers L, Wuytack F, Vanoevelen J. The Ca2+ pumps of the endoplasmic reticulum and Golgi apparatus. Cold Spring Harb Perspect Biol 2011; 3(5): a004184.
[http://dx.doi.org/10.1101/cshperspect.a004184] [PMID: 21441596]
[31]
Gorski PA, Trieber CA, Larivière E, et al. Transmembrane helix 11 is a genuine regulator of the endoplasmic reticulum Ca2+ pump and acts as a functional parallel of β-subunit on α-Na+,K+-ATPase. J Biol Chem 2012; 287(24): 19876-85.
[http://dx.doi.org/10.1074/jbc.M111.335620] [PMID: 22528494]
[32]
Gélébart P, Martin V, Enouf J, Papp B. Identification of a new SERCA2 splice variant regulated during monocytic differentiation. Biochem Biophys Res Commun 2003; 303(2): 676-84.
[http://dx.doi.org/10.1016/S0006-291X(03)00405-4] [PMID: 12659872]
[33]
Park KC, Kim SW, Jeon JY, et al. Survival of cancer stem-like cells under metabolic stress via camk2α-mediated upregulation of sarco/endoplasmic reticulum calcium ATPase expression. Clin Cancer Res 2018; 24(7): 1677-90.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-2219] [PMID: 29279319]
[34]
Seo J, Kim B, Dhanasekaran DN, Tsang BK, Song YS. Curcumin induces apoptosis by inhibiting sarco/endoplasmic reticulum Ca2+ ATPase activity in ovarian cancer cells. Cancer Lett 2016; 371(1): 30-7.
[http://dx.doi.org/10.1016/j.canlet.2015.11.021] [PMID: 26607901]
[35]
Fan L, Li A, Li W, et al. Novel role of Sarco/endoplasmic reticulum calcium ATPase 2 in development of colorectal cancer and its regulation by F36, a curcumin analog. Biomed Pharmacother 2014; 68(8): 1141-8.
[http://dx.doi.org/10.1016/j.biopha.2014.10.014] [PMID: 25458791]
[36]
Sunlu H, Lu M. Mechanism of dihydroartemisinin binding SERCA2b and inducing apoptosis in colorectal cell HCT-116. Zhongguo Yike Daxue Xuebao 2024; 1-6.
[37]
Li W, Ouyang Z, Zhang Q, et al. SBF-1 exerts strong anticervical cancer effect through inducing endoplasmic reticulum stress-associated cell death via targeting sarco/endoplasmic reticulum Ca2+-ATPase 2. Cell Death Dis 2014; 5(12): e1581.
[http://dx.doi.org/10.1038/cddis.2014.538] [PMID: 25522275]
[38]
Yang B, Zhang M, Gao J, et al. Small molecule RL71 targets SERCA2 at a novel site in the treatment of human colorectal cancer. Oncotarget 2015; 6(35): 37613-25.
[http://dx.doi.org/10.18632/oncotarget.6068] [PMID: 26608678]
[39]
Zhang L, Cheng X, Xu S, Bao J, Yu H. Curcumin induces endoplasmic reticulum stress-associated apoptosis in human papillary thyroid carcinoma BCPAP cells via disruption of intracellular calcium homeostasis. Medicine (Baltimore) 2018; 97(24): e11095.
[http://dx.doi.org/10.1097/MD.0000000000011095] [PMID: 29901626]
[40]
Wang L, Wang L, Song R, et al. Targeting sarcoplasmic/endoplasmic reticulum Ca2+-ATPase 2 by curcumin induces ER stress-associated apoptosis for treating human liposarcoma. Mol Cancer Ther 2011; 10(3): 461-71.
[http://dx.doi.org/10.1158/1535-7163.MCT-10-0812] [PMID: 21282356]
[41]
Chen CC, Chen BR, Wang Y, et al. Sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) activity is required for V(D)J recombination. J Exp Med 2021; 218(8): e20201708.
[http://dx.doi.org/10.1084/jem.20201708] [PMID: 34033676]
[42]
Isaacs JT, Brennen WN, Christensen SB, Denmeade SR. Mipsagargin: The beginning—not the end—of thapsigargin prodrug-based cancer therapeutics. Molecules 2021; 26(24): 7469.
[http://dx.doi.org/10.3390/molecules26247469] [PMID: 34946547]
[43]
Chen P, Li Y, Zhou Z, Pan C, Zeng L. Lathyrol promotes ER stress-induced apoptosis and proliferation inhibition in lung cancer cells by targeting SERCA2. Biomed Pharmacother 2023; 158: 114123.
[http://dx.doi.org/10.1016/j.biopha.2022.114123] [PMID: 36521248]
[44]
Wang R, Wang Y, Niu Y, et al. Deep learning-predicted dihydroartemisinin rescues osteoporosis by maintaining mesenchymal stem cell stemness through activating histone 3 lys 9 acetylation. ACS Cent Sci 2023; 9(10): 1927-43.
[http://dx.doi.org/10.1021/acscentsci.3c00794] [PMID: 37901168]
[45]
Lee AY, Park JY, Chun JM, et al. Optimization of extraction condition for alisol B and alisol B acetate in alismatis rhizoma using response surface methodology. J Liq Chromatogr Relat Technol 2013; 36(4): 513-24.
[http://dx.doi.org/10.1080/10826076.2012.668733] [PMID: 23335845]
[46]
Kotha RR, Luthria DL. Curcumin: Biological, pharmaceutical, nutraceutical, and analytical aspects. Molecules 2019; 24(16): 2930.
[http://dx.doi.org/10.3390/molecules24162930] [PMID: 31412624]
[47]
Deepika , Maurya PK. Benefits of quercetin in age-related diseases. Molecules 2022; 27(8): 2498.
[http://dx.doi.org/10.3390/molecules27082498]
[48]
Hossain U, Das AK, Ghosh S, Sil PC. An overview on the role of bioactive α-glucosidase inhibitors in ameliorating diabetic complications. Food Chem Toxicol 2020; 145: 111738.
[http://dx.doi.org/10.1016/j.fct.2020.111738] [PMID: 32916220]
[49]
Zhao Z, Nian M, Qiao H, Yang X, Wu S, Zheng X. Review of bioactivity and structure-activity relationship on baicalein (5,6,7-trihydroxyflavone) and wogonin (5,7-dihydroxy-8-metho- xyflavone) derivatives: Structural modifications inspired from flavonoids in Scutellaria baicalensis. Eur J Med Chem 2022; 243: 114733.
[http://dx.doi.org/10.1016/j.ejmech.2022.114733] [PMID: 36155355]
[50]
Chagas MSS, Behrens MD, Moragas-Tellis CJ, Penedo GXM, Silva AR, Gonçalves-de-Albuquerque CF. Flavonols and flavones as potential anti-inflammatory, antioxidant, and antibacterial compounds. Oxid Med Cell Longev 2022; 2022: 1-21.
[http://dx.doi.org/10.1155/2022/9966750] [PMID: 36111166]
[51]
Kurisawa N, Iwasaki A, Teranuma K, et al. Structural determination, total synthesis, and biological activity of iezoside, a highly potent Ca2+ -ATPase inhibitor from the marine cyanobacterium Leptochromothrix valpauliae. J Am Chem Soc 2022; 144(24): 11019-32.
[http://dx.doi.org/10.1021/jacs.2c04459] [PMID: 35673891]
[52]
Lv X, Zhang W, Xia S, Huang Z, Shi P. Clioquinol inhibits cell growth in a SERCA2-dependent manner. J Biochem Mol Toxicol 2021; 35(5): e22727.
[http://dx.doi.org/10.1002/jbt.22727] [PMID: 33511738]
[53]
Johnson AJ, Hsu AL, Lin HP, Song X, Chen CS. The cyclo-oxygenase-2 inhibitor celecoxib perturbs intracellular calcium by inhibiting endoplasmic reticulum Ca2+-ATPases: A plausible link with its anti-tumour effect and cardiovascular risks. Biochem J 2002; 366(3): 831-7.
[http://dx.doi.org/10.1042/bj20020279] [PMID: 12076251]
[54]
Wang A, Zheng Y, Zhu W, Yang L, Yang Y, Peng J. Melittin-based nano-delivery systems for cancer therapy. Biomolecules 2022; 12(1): 118.
[http://dx.doi.org/10.3390/biom12010118] [PMID: 35053266]
[55]
Iwasaki A, Ohno O, Katsuyama S, et al. Identification of a molecular target of kurahyne, an apoptosis-inducing lipopeptide from marine cyanobacterial assemblages. Bioorg Med Chem Lett 2015; 25(22): 5295-8.
[http://dx.doi.org/10.1016/j.bmcl.2015.09.044] [PMID: 26428873]
[56]
Horng CT, Chiang NN, Chen IL, et al. Effect of clotrimazole on cytosolic Ca2+ rise and viability in HA59T human hepatoma cells. J Recept Signal Transduct Res 2013; 33(2): 89-95.
[http://dx.doi.org/10.3109/10799893.2013.764321] [PMID: 23384009]
[57]
Jaskulska A, Janecka AE, Gach-Janczak K. Thapsigargin—from traditional medicine to anticancer drug. Int J Mol Sci 2020; 22(1): 4.
[http://dx.doi.org/10.3390/ijms22010004] [PMID: 33374919]
[58]
Peterková L, Kmoníčková E, Ruml T, Rimpelová S. Sarco/endoplasmic reticulum calcium atpase inhibitors: beyond anticancer perspective. J Med Chem 2020; 63(5): 1937-63.
[http://dx.doi.org/10.1021/acs.jmedchem.9b01509] [PMID: 32030976]
[59]
Law BYK, Wang M, Ma DL, et al. Alisol B, a novel inhibitor of the sarcoplasmic/endoplasmic reticulum Ca2+ ATPase pump, induces autophagy, endoplasmic reticulum stress, and apoptosis. Mol Cancer Ther 2010; 9(3): 718-30.
[http://dx.doi.org/10.1158/1535-7163.MCT-09-0700] [PMID: 20197400]
[60]
Zhang J, Li Y, Wang JG, Feng JY, Huang GD, Luo CG. Dihydroartemisinin affects STAT3/DDA1 signaling pathway and reverses breast cancer resistance to cisplatin. Am J Chin Med 2023; 51(2): 445-59.
[http://dx.doi.org/10.1142/S0192415X23500234] [PMID: 36891981]
[61]
Wang Y, Yang Z, Zhu W, et al. Dihydroartemisinin inhibited stem cell-like properties and enhanced oxaliplatin sensitivity of colorectal cancer via AKT/mTOR signaling. Drug Dev Res 2023; 84(5): 988-98.
[http://dx.doi.org/10.1002/ddr.22067] [PMID: 37132439]
[62]
Ma Y, Zhang P, Zhang Q, et al. Dihydroartemisinin suppresses proliferation, migration, the Wnt/β-catenin pathway and EMT via TNKS in gastric cancer. Oncol Lett 2021; 22(4): 688.
[http://dx.doi.org/10.3892/ol.2021.12949] [PMID: 34457043]
[63]
Dai X, Chen W, Qiao Y, et al. Dihydroartemisinin inhibits the development of colorectal cancer by GSK-3β/TCF7/MMP9 pathway and synergies with capecitabine. Cancer Lett 2024; 582: 216596.
[http://dx.doi.org/10.1016/j.canlet.2023.216596] [PMID: 38101610]
[64]
Imran M, Rauf A, Abu-Izneid T, et al. Luteolin, a flavonoid, as an anticancer agent: A review. Biomed Pharmacother 2019; 112: 108612.
[http://dx.doi.org/10.1016/j.biopha.2019.108612] [PMID: 30798142]
[65]
Kuhar M, Sen S, Singh N. Role of mitochondria in quercetin-enhanced chemotherapeutic response in human non-small cell lung carcinoma H-520 cells. Anticancer Res 2006; 26(2A): 1297-303.
[PMID: 16619537]
[66]
Ogunbayo OA, Harris RM, Waring RH, Kirk CJ, Michelangeli F. Inhibition of the sarcoplasmic/endoplasmic reticulum Ca2+ -ATPase by flavonoids: A quantitative structure-activity relationship study. IUBMB Life 2008; 60(12): 853-8.
[http://dx.doi.org/10.1002/iub.132] [PMID: 18785622]
[67]
Luo Y, Xu C, Luo B, Liang G, Zhang Q. Melittin treatment prevents colorectal cancer from progressing in mice through ER stress-mediated apoptosis. J Pharm Pharmacol 2023; 75(5): 645-54.
[http://dx.doi.org/10.1093/jpp/rgad008] [PMID: 36966363]
[68]
Bartolommei G, Tadini-Buoninsegni F, Hua S, Moncelli MR, Inesi G, Guidelli R. Clotrimazole inhibits the Ca2+-ATPase (SERCA) by interfering with Ca2+ binding and favoring the E2 conformation. J Biol Chem 2006; 281(14): 9547-51.
[http://dx.doi.org/10.1074/jbc.M510550200] [PMID: 16452481]
[69]
Huang H, Chen AY, Ye X, Guan R, Rankin GO, Chen YC. Galangin, a flavonoid from lesser galangal, induced apoptosis via p53-dependent pathway in ovarian cancer cells. Molecules 2020; 25(7): 1579.
[http://dx.doi.org/10.3390/molecules25071579] [PMID: 32235536]
[70]
Howells LM, Iwuji COO, Irving GRB, et al. Curcumin combined with FOLFOX chemotherapy is safe and tolerable in patients with metastatic colorectal cancer in a randomized phase IIa trial. J Nutr 2019; 149(7): 1133-9.
[http://dx.doi.org/10.1093/jn/nxz029] [PMID: 31132111]
[71]
Søhoel H, Liljefors T, Ley SV, et al. Total synthesis of two novel subpicomolar sarco/endoplasmatic reticulum Ca2+-ATPase inhibitors designed by an analysis of the binding site of thapsigargin. J Med Chem 2005; 48(22): 7005-11.
[http://dx.doi.org/10.1021/jm058036v] [PMID: 16250659]
[72]
Lindner P, Christensen SB, Nissen P, Møller JV, Engedal N. Cell death induced by the ER stressor thapsigargin involves death receptor 5, a non-autophagic function of MAP1LC3B, and distinct contributions from unfolded protein response components. Cell Commun Signal 2020; 18(1): 12.
[http://dx.doi.org/10.1186/s12964-019-0499-z] [PMID: 31987044]
[73]
Zhang J, Huang W, Sun H, et al. Structure identification and in vitro anticancer activity of lathyrol-3-phenylacetate-5,15-diacetate. Molecules 2017; 22(9): 1412.
[http://dx.doi.org/10.3390/molecules22091412] [PMID: 28841191]
[74]
Zhou XW, Tan WF, Xie FY, Xin B, Chen J. Research progress on anti-cancer pharmacological mechanism of dihydroartemisinin. J Pharm Pract 2019; 37(3): 206-11.
[75]
Mu D. Study on the anti-lung cancer effect and mechanism of dihydroartemisinin. Thesis, Fourth military medical university of chinese 2008.
[76]
Ogunbayo OA, Michelangeli F. Related flavonoids cause cooperative inhibition of the sarcoplasmic reticulum Ca2+ ATP ase by multimode mechanisms. FEBS J 2014; 281(3): 766-77.
[http://dx.doi.org/10.1111/febs.12621] [PMID: 24238016]
[77]
Lin YT, Yang JS, Lin HJ, et al. Baicalein induces apoptosis in SCC-4 human tongue cancer cells via a Ca2+-dependent mitochondrial pathway. In vivo 2007; 21(6): 1053-8.
[PMID: 18210755]
[78]
Li KS, He ML, Pi RB, Liu AM. Research progress on anti-cancer mechanism of classical antibacterial chloroiodoquine. Zhongguo Xin Yao Zazhi 2015; 24(09): 1002-6.
[79]
White MC, Johnson GG, Zhang W, Hobrath JV, Piazza GA, Grimaldi M. Sulindac sulfide inhibits sarcoendoplasmic reticulum Ca2+ ATPase, induces endoplasmic reticulum stress response, and exerts toxicity in glioma cells: Relevant similarities to and important differences from celecoxib. J Neurosci Res 2013; 91(3): 393-406.
[http://dx.doi.org/10.1002/jnr.23169] [PMID: 23280445]
[80]
Voss JC, Mahaney JE, Thomas DD. Mechanism of Ca-ATPase inhibition by melittin in skeletal sarcoplasmic reticulum. Biochemistry 1995; 34(3): 930-9.
[http://dx.doi.org/10.1021/bi00003a027] [PMID: 7827051]
[81]
Senft D, Ronai ZA. UPR, autophagy, and mitochondria crosstalk underlies the ER stress response. Trends Biochem Sci 2015; 40(3): 141-8.
[http://dx.doi.org/10.1016/j.tibs.2015.01.002] [PMID: 25656104]
[82]
Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87(1): 99-163.
[http://dx.doi.org/10.1152/physrev.00013.2006] [PMID: 17237344]
[83]
Chipuk JE, Green DR. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol 2008; 18(4): 157-64.
[http://dx.doi.org/10.1016/j.tcb.2008.01.007] [PMID: 18314333]
[84]
Li Z, Zhang R, Yin X, et al. Realgar (As4S4), a traditional Chinese medicine, induces acute promyelocytic leukemia cell death via the Bcl-2/Bax/Cyt-C/AIF signaling pathway in vitro. Aging (Albany NY) 2022; 14(17): 7109-25.
[http://dx.doi.org/10.18632/aging.204281] [PMID: 36098742]
[85]
Chen X, Li S, Zeng Z, et al. Notch1 signalling inhibits apoptosis of human dental follicle stem cells via both the cytoplasmic mitochondrial pathway and nuclear transcription regulation. Int J Biochem Cell Biol 2017; 82: 18-27.
[http://dx.doi.org/10.1016/j.biocel.2016.11.013] [PMID: 27888063]
[86]
Song M, Zhang J, Huo S, Zhang X, Cui Y, Li Y. Mitophagy alleviates AIF-mediated spleen apoptosis induced by AlCl3 through Parkin stabilization in mice. Food Chem Toxicol 2023; 176: 113762.
[http://dx.doi.org/10.1016/j.fct.2023.113762] [PMID: 37028746]
[87]
Zong L, Liang Z. Apoptosis-inducing factor: A mitochondrial protein associated with metabolic diseases — A narrative review. Cardiovasc Diagn Ther 2023; 12(3): 609-22.
[http://dx.doi.org/10.21037/cdt-23-123] [PMID: 37405018]
[88]
Zhang J, Guo J, Yang N, Huang Y, Hu T, Rao C. Endoplasmic reticulum stress-mediated cell death in liver injury. Cell Death Dis 2022; 13(12): 1051.
[http://dx.doi.org/10.1038/s41419-022-05444-x] [PMID: 36535923]
[89]
Rakesh R, PriyaDharshini LC, Sakthivel KM, Rasmi RR. Role and regulation of autophagy in cancer. Biochim Biophys Acta Mol Basis Dis 2022; 1868(7): 166400.
[http://dx.doi.org/10.1016/j.bbadis.2022.166400] [PMID: 35341960]
[90]
Da Costa MacHado AK, MacHado CB, De Pinho Pessoa FMC, et al. Development and clinical applications of PI3K/AKT/mTOR pathway inhibitors as a therapeutic option for leukemias. Cancer Diagn Progn 2024; 4(1): 9-24.
[http://dx.doi.org/10.21873/cdp.10279] [PMID: 38173664]
[91]
Liao WT, Chiang YJ, Yang-Yen HF, Hsu LC, Chang ZF, Yen JJY. Correction: CBAP regulates the function of Akt-associated TSC protein complexes to modulate mTORC1 signaling. J Biol Chem 2024; 300(2): 105686.
[http://dx.doi.org/10.1016/j.jbc.2024.105686] [PMID: 38290174]
[92]
He Z, Xu Y, Rao Z, et al. The role of α7-nAChR-mediated PI3K/AKT pathway in lung cancer induced by nicotine. Sci Total Environ 2024; 912: 169604.
[http://dx.doi.org/10.1016/j.scitotenv.2023.169604] [PMID: 38157907]
[93]
Chen L, Zhu L, Shi H, et al. Endoplasmic reticulum stress-mediated autophagy alleviates lipopolysaccharide-induced nucleus pulposus cell pyroptosis by inhibiting CHOP signaling in vitro. J Biochem Mol Toxicol 2024; 38(1): e23523.
[http://dx.doi.org/10.1002/jbt.23523] [PMID: 37654027]
[94]
Khezri MR, Hsueh HY, Mohammadipanah S, Khalili Fard J, Ghasemnejad-Berenji M. The interplay between the PI3K/AKT pathway and circadian clock in physiologic and cancer-related pathologic conditions. Cell Prolif 2024; 57(7): e13608.
[http://dx.doi.org/10.1111/cpr.13608] [PMID: 38336976]
[95]
Wiseman RL, Mesgarzadeh JS, Hendershot LM. Reshaping endoplasmic reticulum quality control through the unfolded protein response. Mol Cell 2022; 82(8): 1477-91.
[http://dx.doi.org/10.1016/j.molcel.2022.03.025] [PMID: 35452616]
[96]
Hu X, Pan G, Luo J, et al. Kuwanon H inhibits melanoma growth through cytotoxic endoplasmic reticulum stress and impaired autophagy flux. J Agric Food Chem 2023; 71(37): 13768-82.
[http://dx.doi.org/10.1021/acs.jafc.3c02257] [PMID: 37672659]
[97]
Ge Y, Zhou M, Chen C, Wu X, Wang X. Role of AMPK mediated pathways in autophagy and aging. Biochimie 2022; 195: 100-13.
[http://dx.doi.org/10.1016/j.biochi.2021.11.008] [PMID: 34838647]
[98]
Mihaylova MM, Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 2011; 13(9): 1016-23.
[http://dx.doi.org/10.1038/ncb2329] [PMID: 21892142]
[99]
Herzig S, Shaw RJ. AMPK: Guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol 2018; 19(2): 121-35.
[http://dx.doi.org/10.1038/nrm.2017.95] [PMID: 28974774]
[100]
Zhang J, Yang L, Han X, et al. Endoplasmic reticulum stress in hepatic stellate cells induced by tunicamycin promotes apoptosis and cell cycle arrest. Xibao Yu Fenzi Mianyixue Zazhi 2021; 37(9): 794-800.
[PMID: 34533126]
[101]
Khan MGM, Wang Y. Cell cycle-related clinical applications. Methods Mol Biol 2022; 2579: 35-46.
[http://dx.doi.org/10.1007/978-1-0716-2736-5_3] [PMID: 36045196]
[102]
Heber-Katz E, Zhang Y, Bedelbaeva K, Song F, Chen X, Stocum DL. Cell cycle regulation and regeneration. Curr Top Microbiol Immunol 2012; 367: 253-76.
[http://dx.doi.org/10.1007/82_2012_294] [PMID: 23263201]
[103]
Kahl CR, Means AR. Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr Rev 2003; 24(6): 719-36.
[http://dx.doi.org/10.1210/er.2003-0008] [PMID: 14671000]
[104]
Huang Y, Yang M, Huang W. 14-3-3 σ: A potential biomolecule for cancer therapy. Clin Chim Acta 2020; 511: 50-8.
[http://dx.doi.org/10.1016/j.cca.2020.09.009] [PMID: 32950519]
[105]
Bourougaa K, Naski N, Boularan C, et al. Endoplasmic reticulum stress induces G2 cell-cycle arrest via mRNA translation of the p53 isoform p53/47. Mol Cell 2010; 38(1): 78-88.
[http://dx.doi.org/10.1016/j.molcel.2010.01.041] [PMID: 20385091]
[106]
Agarwal P, DeInnocentes P, Bird RC. Evaluation of 14-3-3 sigma as a potential partner of p16 in quiescence and differentiation. in vitro Cell Dev Biol Anim 2018; 54(9): 658-65.
[http://dx.doi.org/10.1007/s11626-018-0291-1] [PMID: 30168069]
[107]
Chan TA, Hermeking H, Lengauer C, Kinzler KW, Vogelstein B. 14-3-3σ is required to prevent mitotic catastrophe after DNA damage. Nature 1999; 401(6753): 616-20.
[http://dx.doi.org/10.1038/44188] [PMID: 10524633]