The Emerging Potential of Parthenolide Nanoformulations in Tumor Therapy

References

• Végh K, Alberti Á, Riethmüller E, Tóth A, Béni S, Kéry Á. Supercritical fluid extraction and convergence chromatographic determination of parthenolide in Tanacetum parthenium L.: experimental design, modeling and optimization. J Supercrit Fluids. 2014;95:84–91. doi:10.1016/j.supflu.2014.07.029
   Web of Science ®Google Scholar
• Alam P, Siddiqui NA, Rehman MT, et al. Box-Behnken Design (BBD)-Based optimization of microwave-assisted extraction of parthenolide from the stems of tarconanthus camphoratus and cytotoxic analysis. Molecules. 2021;26(7):1876. doi:10.3390/molecules26071876
   PubMed Web of Science ®Google Scholar
• Ghantous A, Sinjab A, Herceg Z, Darwiche N. Parthenolide: from plant shoots to cancer roots. Drug Discov Today. 2013;18(17–18):894–905. doi:10.1016/j.drudis.2013.05.005
   PubMed Web of Science ®Google Scholar
• Freund RRA, Gobrecht P, Fischer D, Arndt HD. Advances in chemistry and bioactivity of parthenolide. Nat Prod Rep. 2020;37(4):541–565. doi:10.1039/C9NP00049F
   PubMed Web of Science ®Google Scholar
• Siveen KS, Uddin S, Mohammad RM. Targeting acute myeloid leukemia stem cell signaling by natural products. Mol Cancer. 2017;16(1):13. doi:10.1186/s12943-016-0571-x
   PubMedGoogle Scholar
• Araujo TG, Vecchi L, Lima P, et al. Parthenolide and its analogues: a new potential strategy for the treatment of triple-negative breast tumors. Curr Med Chem. 2020;27(39):6628–6642. doi:10.2174/0929867326666190816230121
   PubMed Web of Science ®Google Scholar
• Dandawate PR, Subramaniam D, Jensen RA, Anant S. Targeting cancer stem cells and signaling pathways by phytochemicals: novel approach for breast cancer therapy. Semin Cancer Biol. 2016;40–41:192–208. doi:10.1016/j.semcancer.2016.09.001
   PubMed Web of Science ®Google Scholar
• Ren Y, Yu J, Kinghorn AD. Development of anticancer agents from plant-derived sesquiterpene lactones. Curr Med Chem. 2016;23(23):2397–2420. doi:10.2174/0929867323666160510123255
   PubMed Web of Science ®Google Scholar
• Mathema VB, Koh YS, Thakuri BC, Sillanpaa M. Parthenolide, a sesquiterpene lactone, expresses multiple anti-cancer and anti-inflammatory activities. Inflammation. 2012;35(2):560–565. doi:10.1007/s10753-011-9346-0
   PubMed Web of Science ®Google Scholar
• Ghantous A, Gali-Muhtasib H, Vuorela H, Saliba NA, Darwiche N. What made sesquiterpene lactones reach cancer clinical trials? Drug Discov Today. 2010;15(15–16):668–678. doi:10.1016/j.drudis.2010.06.002
   PubMed Web of Science ®Google Scholar
• Koprowska K, Czyz M. [Molecular mechanisms of parthenolide’s action: old drug with a new face]. Postepy Hig Med Dosw. 2010;64:100–114. Norwegian.
   Web of Science ®Google Scholar
• Kreuger MR, Grootjans S, Biavatti MW, Vandenabeele P, D’Herde K. Sesquiterpene lactones as drugs with multiple targets in cancer treatment: focus on parthenolide. Anticancer Drugs. 2012;23(9):883–896. doi:10.1097/CAD.0b013e328356cad9
   PubMed Web of Science ®Google Scholar
• Wyrebska A, Gach K, Janecka A. Combined effect of parthenolide and various anti-cancer drugs or anticancer candidate substances on malignant cells in vitro and in vivo. Mini Rev Med Chem. 2014;14(3):222–228. doi:10.2174/1389557514666140219113509
   PubMed Web of Science ®Google Scholar
• Sztiller-Sikorska M, Czyz M. Parthenolide as cooperating agent for anti-cancer treatment of various malignancies. Pharmaceuticals. 2020;13(8):194. doi:10.3390/ph13080194
   Web of Science ®Google Scholar
• Pordanjani SM, Hosseinimehr SJ. The role of NF-kB inhibitors in cell response to radiation. Curr Med Chem. 2016;23(34):3951–3963. doi:10.2174/0929867323666160824162718
   PubMed Web of Science ®Google Scholar
• Lesiak K, Koprowska K, Zalesna I, Nejc D, Duchler M, Czyz M. Parthenolide, a sesquiterpene lactone from the medical herb feverfew, shows anticancer activity against human melanoma cells in vitro. Melanoma Res. 2010;20(1):21–34. doi:10.1097/CMR.0b013e328333bbe4
   PubMed Web of Science ®Google Scholar
• Nasim S, Crooks PA. Antileukemic activity of aminoparthenolide analogs. Bioorg Med Chem Lett. 2008;18(14):3870–3873. doi:10.1016/j.bmcl.2008.06.050
   PubMed Web of Science ®Google Scholar
• Ren Y, Kinghorn AD. Development of potential antitumor agents from the scaffolds of plant-derived terpenoid lactones. J Med Chem. 2020;63(24):15410–15448. doi:10.1021/acs.jmedchem.0c01449
   PubMed Web of Science ®Google Scholar
• Guzman ML, Rossi RM, Neelakantan S, et al. An orally bioavailable parthenolide analog selectively eradicates acute myelogenous leukemia stem and progenitor cells. Blood. 2007;110(13):4427–4435. doi:10.1182/blood-2007-05-090621
   PubMed Web of Science ®Google Scholar
• Wu D, Si M, Xue HY, Wong HL. Nanomedicine applications in the treatment of breast cancer: current state of the art. Int J Nanomedicine. 2017;12:5879–5892. doi:10.2147/IJN.S123437
   PubMed Web of Science ®Google Scholar
• Zhang J, Tang H, Liu Z, Chen B. Effects of major parameters of nanoparticles on their physical and chemical properties and recent application of nanodrug delivery system in targeted chemotherapy. Int J Nanomedicine. 2017;12:8483–8493. doi:10.2147/IJN.S148359
   PubMed Web of Science ®Google Scholar
• Jasinski DL, Li H, Guo P. The effect of size and shape of RNA nanoparticles on biodistribution. Mol Ther. 2018;26(3):784–792. doi:10.1016/j.ymthe.2017.12.018
   PubMed Web of Science ®Google Scholar
• Torchilin V. Tumor delivery of macromolecular drugs based on the EPR effect. Adv Drug Deliv Rev. 2011;63(3):131–135. doi:10.1016/j.addr.2010.03.011
   PubMed Web of Science ®Google Scholar
• Li X, Kong L, Yang Q, et al. Parthenolide inhibits ubiquitin-specific peptidase 7 (USP7), Wnt signaling, and colorectal cancer cell growth. J Biol Chem. 2020;295(11):3576–3589. doi:10.1074/jbc.RA119.011396
   PubMed Web of Science ®Google Scholar
• Zhang S, Ju X, Yang Q, et al. USP47 maintains the stemness of colorectal cancer cells and is inhibited by parthenolide. Biochem Biophys Res Commun. 2021;562:21–28. doi:10.1016/j.bbrc.2021.05.017
   PubMed Web of Science ®Google Scholar
• Ai XY, Zhang H, Gao SY, et al. Sesquiterpene binding Gly-Leu-Ser/Lys-”co-adaptation pocket” to inhibit lung cancer cell epithelial-mesenchymal transition. Oncotarget. 2017;8(41):70192–70203. doi:10.18632/oncotarget.19599
   PubMedGoogle Scholar
• Li X, Huang R, Li M, et al. Parthenolide inhibits the growth of non-small cell lung cancer by targeting epidermal growth factor receptor. Cancer Cell Int. 2020;20(1):561. doi:10.1186/s12935-020-01658-1
   PubMed Web of Science ®Google Scholar
• Garcia-Pineres AJ, Castro V, Mora G, et al. Cysteine 38 in p65/NF-kappaB plays a crucial role in DNA binding inhibition by sesquiterpene lactones. J Biol Chem. 2001;276(43):39713–39720. doi:10.1074/jbc.M101985200
   PubMed Web of Science ®Google Scholar
• Kwok BH, Koh B, Ndubuisi MI, Elofsson M, Crews CM. The anti-inflammatory natural product parthenolide from the medicinal herb Feverfew directly binds to and inhibits IkappaB kinase. Chem Biol. 2001;8(8):759–766. doi:10.1016/S1074-5521(01)00049-7
   PubMedGoogle Scholar
• Kong FC, Zhang JQ, Zeng C, et al. Inhibitory effects of parthenolide on the activity of NF-kappaB in multiple myeloma via targeting TRAF6. J Huazhong Univ Sci Technolog Med Sci. 2015;35(3):343–349. doi:10.1007/s11596-015-1435-0
   PubMedGoogle Scholar
• Kim SL, Park YR, Lee ST, Kim SW. Parthenolide suppresses hypoxia-inducible factor-1alpha signaling and hypoxia induced epithelial-mesenchymal transition in colorectal cancer. Int J Oncol. 2017;51(6):1809–1820. doi:10.3892/ijo.2017.4166
   PubMed Web of Science ®Google Scholar
• Zhu X, Yuan C, Tian C, et al. The plant sesquiterpene lactone parthenolide inhibits Wnt/beta-catenin signaling by blocking synthesis of the transcriptional regulators TCF4/LEF1. J Biol Chem. 2018;293(14):5335–5344. doi:10.1074/jbc.M117.819300
   PubMed Web of Science ®Google Scholar
• Berdan CA, Ho R, Lehtola HS, et al. Parthenolide covalently targets and inhibits focal adhesion kinase in breast cancer cells. Cell Chem Biol. 2019;26(7):1027–1035 e1022. doi:10.1016/j.chembiol.2019.03.016
   PubMed Web of Science ®Google Scholar
• Liu M, Xiao C, Sun M, Tan M, Hu L, Yu Q. Parthenolide inhibits STAT3 signaling by covalently targeting janus kinases. Molecules. 2018;23(6):1478.
   PubMed Web of Science ®Google Scholar
• Gopal YN, Chanchorn E, Van Dyke MW. Parthenolide promotes the ubiquitination of MDM2 and activates p53 cellular functions. Mol Cancer Ther. 2009;8(3):552–562. doi:10.1158/1535-7163.MCT-08-0661
   PubMed Web of Science ®Google Scholar
• Tavana O, Gu W. Modulation of the p53/MDM2 interplay by HAUSP inhibitors. J Mol Cell Biol. 2017;9(1):45–52. doi:10.1093/jmcb/mjw049
   PubMed Web of Science ®Google Scholar
• Colleran A, Collins PE, O’Carroll C, et al. Deubiquitination of NF-kappaB by Ubiquitin-Specific Protease-7 promotes transcription. Proc Natl Acad Sci U S A. 2013;110(2):618–623. doi:10.1073/pnas.1208446110
   PubMed Web of Science ®Google Scholar
• Zhang S, Lin ZN, Yang CF, Shi X, Ong CN, Shen HM. Suppressed NF-kappaB and sustained JNK activation contribute to the sensitization effect of parthenolide to TNF-alpha-induced apoptosis in human cancer cells. Carcinogenesis. 2004;25(11):2191–2199. doi:10.1093/carcin/bgh234
   PubMed Web of Science ®Google Scholar
• Nakshatri H, Rice SE, Bhat-Nakshatri P. Antitumor agent parthenolide reverses resistance of breast cancer cells to tumor necrosis factor-related apoptosis-inducing ligand through sustained activation of c-Jun N-terminal kinase. Oncogene. 2004;23(44):7330–7344. doi:10.1038/sj.onc.1207995
   PubMed Web of Science ®Google Scholar
• D’Anneo A, Carlisi D, Lauricella M, et al. Parthenolide generates reactive oxygen species and autophagy in MDA-MB231 cells. A soluble parthenolide analogue inhibits tumour growth and metastasis in a xenograft model of breast cancer. Cell Death Dis. 2013;4:e891. doi:10.1038/cddis.2013.415
   PubMed Web of Science ®Google Scholar
• Duan D, Zhang J, Yao J, Liu Y, Fang J. Targeting thioredoxin reductase by parthenolide contributes to inducing apoptosis of hela cells. J Biol Chem. 2016;291(19):10021–10031. doi:10.1074/jbc.M115.700591
   PubMed Web of Science ®Google Scholar
• Pei S, Minhajuddin M, Callahan KP, et al. Targeting aberrant glutathione metabolism to eradicate human acute myelogenous leukemia cells. J Biol Chem. 2013;288(47):33542–33558. doi:10.1074/jbc.M113.511170
   PubMed Web of Science ®Google Scholar
• Yang C, Yang QO, Kong QJ, Yuan W, Ou Yang YP. Parthenolide induces reactive oxygen species-mediated autophagic cell death in human osteosarcoma cells. Cell Physiol Biochem. 2016;40(1–2):146–154. doi:10.1159/000452532
   PubMedGoogle Scholar
• Xu Y, Fang F, Miriyala S, et al. KEAP1 is a redox sensitive target that arbitrates the opposing radiosensitive effects of parthenolide in normal and cancer cells. Cancer Res. 2013;73(14):4406–4417. doi:10.1158/0008-5472.CAN-12-4297
   PubMed Web of Science ®Google Scholar
• Liu Z, Liu S, Xie Z, et al. Modulation of DNA methylation by a sesquiterpene lactone parthenolide. J Pharmacol Exp Ther. 2009;329(2):505–514. doi:10.1124/jpet.108.147934
   PubMed Web of Science ®Google Scholar
• Gopal YN, Arora TS, Van Dyke MW. Parthenolide specifically depletes histone deacetylase 1 protein and induces cell death through ataxia telangiectasia mutated. Chem Biol. 2007;14(7):813–823. doi:10.1016/j.chembiol.2007.06.007
   PubMedGoogle Scholar
• Nakshatri H, Appaiah HN, Anjanappa M, et al. NF-kappaB-dependent and -independent epigenetic modulation using the novel anti-cancer agent DMAPT. Cell Death Dis. 2015;6:e1608. doi:10.1038/cddis.2014.569
   PubMed Web of Science ®Google Scholar
• Fonrose X, Ausseil F, Soleilhac E, et al. Parthenolide inhibits tubulin carboxypeptidase activity. Cancer Res. 2007;67(7):3371–3378. doi:10.1158/0008-5472.CAN-06-3732
   PubMed Web of Science ®Google Scholar
• Whipple RA, Vitolo MI, Boggs AE, Charpentier MS, Thompson K, Martin SS. Parthenolide and costunolide reduce microtentacles and tumor cell attachment by selectively targeting detyrosinated tubulin independent from NF-kappaB inhibition. Breast Cancer Res. 2013;15(5):R83. doi:10.1186/bcr3477
   PubMed Web of Science ®Google Scholar
• Carlisi D, Lauricella M, D’Anneo A, et al. Parthenolide and its soluble analogues: multitasking compounds with antitumor properties. Biomedicines. 2022;10(2):514. doi:10.3390/biomedicines10020514
   PubMed Web of Science ®Google Scholar
• Marino S, Bishop RT, Carrasco G, Logan JG, Li B, Idris AI. Pharmacological inhibition of NFkappaB reduces prostate cancer related osteoclastogenesis in vitro and osteolysis ex vivo. Calcif Tissue Int. 2019;105(2):193–204. doi:10.1007/s00223-019-00538-9
   PubMed Web of Science ®Google Scholar
• Ge W, Liu Z, Sun Y, et al. Design and synthesis of parthenolide-SAHA hybrids for intervention of drug-resistant acute myeloid leukemia. Bioorg Chem. 2019;87:699–713. doi:10.1016/j.bioorg.2019.03.056
   PubMed Web of Science ®Google Scholar
• Mehri S, Mohammadi S, Nikbakht M, Sahmani M, Zahedpanah M. Osteopontin siRNA does not confer resistance to toxic effects of parthenolide in Jurkat cells. Exp Oncol. 2020;42(3):188–191. doi:10.32471/exp-oncology.2312-8852.vol-42-no-3.15180
   PubMedGoogle Scholar
• Ge W, Hao X, Han F, et al. Synthesis and structure-activity relationship studies of parthenolide derivatives as potential anti-triple negative breast cancer agents. Eur J Med Chem. 2019;166:445–469. doi:10.1016/j.ejmech.2019.01.058
   PubMed Web of Science ®Google Scholar
• De Blasio A, Di Fiore R, Pratelli G, et al. A loop involving NRF2, miR-29b-1-5p and AKT, regulates cell fate of MDA-MB-231 triple-negative breast cancer cells. J Cell Physiol. 2020;235(2):629–637. doi:10.1002/jcp.29062
   PubMed Web of Science ®Google Scholar
• Dawood M, Ooko E, Efferth T. Collateral sensitivity of parthenolide via NF-kappaB and HIF-alpha inhibition and epigenetic changes in drug-resistant cancer cell lines. Front Pharmacol. 2019;10:542. doi:10.3389/fphar.2019.00542
   PubMed Web of Science ®Google Scholar
• Ding Y, Li S, Ge W, et al. Design and synthesis of parthenolide and 5-fluorouracil conjugates as potential anticancer agents against drug resistant hepatocellular carcinoma. Eur J Med Chem. 2019;183:111706. doi:10.1016/j.ejmech.2019.111706
   PubMed Web of Science ®Google Scholar
• Sun L, Yuan W, Wen G, et al. Parthenolide inhibits human lung cancer cell growth by modulating the IGF1R/PI3K/Akt signaling pathway. Oncol Rep. 2020;44(3):1184–1193. doi:10.3892/or.2020.7649
   PubMed Web of Science ®Google Scholar
• Luo Q, Wu X, Chang W, et al. ARID1A hypermethylation disrupts transcriptional homeostasis to promote squamous cell carcinoma progression. Cancer Res. 2020;80(3):406–417. doi:10.1158/0008-5472.CAN-18-2446
   PubMed Web of Science ®Google Scholar
• Che ST, Bie L, Li X, Qi H, Yu P, Zuo L. Parthenolide inhibits the proliferation and induces the apoptosis of human uveal melanoma cells. Int J Ophthalmol. 2019;12(10):1531–1538. doi:10.18240/ijo.2019.10.03
   PubMed Web of Science ®Google Scholar
• Tang TK, Chiu SC, Lin CW, Su MJ, Liao MH. Induction of survivin inhibition, G(2)/M cell cycle arrest and autophagic on cell death in human malignant glioblastoma cells. Chin J Physiol. 2015;58(2):95–103. doi:10.4077/CJP.2015.BAC267
   PubMed Web of Science ®Google Scholar
• Gali-Muhtasib H, Hmadi R, Kareh M, Tohme R, Darwiche N. Cell death mechanisms of plant-derived anticancer drugs: beyond apoptosis. Apoptosis. 2015;20(12):1531–1562. doi:10.1007/s10495-015-1169-2
   PubMed Web of Science ®Google Scholar
• Singh R, Letai A, Sarosiek K. Regulation of apoptosis in health and disease: the balancing act of BCL-2 family proteins. Nat Rev Mol Cell Biol. 2019;20(3):175–193. doi:10.1038/s41580-018-0089-8
   PubMed Web of Science ®Google Scholar
• Yi J, Wang L, Wang XY, et al. Suppression of aberrant activation of NF-kappaB pathway in drug-resistant leukemia stem cells contributes to parthenolide-potentiated reversal of drug resistance in leukemia. J Cancer. 2021;12(18):5519–5529. doi:10.7150/jca.52641
   PubMed Web of Science ®Google Scholar
• Kwak SW, Park ES, Lee CS. Parthenolide induces apoptosis by activating the mitochondrial and death receptor pathways and inhibits FAK-mediated cell invasion. Mol Cell Biochem. 2014;385(1–2):133–144. doi:10.1007/s11010-013-1822-4
   PubMed Web of Science ®Google Scholar
• Carlisi D, D’Anneo A, Angileri L, et al. Parthenolide sensitizes hepatocellular carcinoma cells to TRAIL by inducing the expression of death receptors through inhibition of STAT3 activation. J Cell Physiol. 2011;226(6):1632–1641. doi:10.1002/jcp.22494
   PubMed Web of Science ®Google Scholar
• Dai Y, Guzman ML, Chen S, et al. The NF (Nuclear factor)-kappaB inhibitor parthenolide interacts with histone deacetylase inhibitors to induce MKK7/JNK1-dependent apoptosis in human acute myeloid leukaemia cells. Br J Haematol. 2010;151(1):70–83. doi:10.1111/j.1365-2141.2010.08319.x
   PubMed Web of Science ®Google Scholar
• Talib WH, Al Kury LT. Parthenolide inhibits tumor-promoting effects of nicotine in lung cancer by inducing P53 - dependent apoptosis and inhibiting VEGF expression. Biomed Pharmacother. 2018;107:1488–1495. doi:10.1016/j.biopha.2018.08.139
   PubMed Web of Science ®Google Scholar
• Li H, Lu H, Lv M, Wang Q, Sun Y. Parthenolide facilitates apoptosis and reverses drug-resistance of human gastric carcinoma cells by inhibiting the STAT3 signaling pathway. Oncol Lett. 2018;15(3):3572–3579. doi:10.3892/ol.2018.7739
   PubMed Web of Science ®Google Scholar
• Yuan L, Wang Z, Zhang D, Wang J. Metabonomic study of the intervention effects of Parthenolide on anti-thyroid cancer activity. J Chromatogr B Analyt Technol Biomed Life Sci. 2020;1150:122179. doi:10.1016/j.jchromb.2020.122179
   PubMed Web of Science ®Google Scholar
• Provance OK, Geanes ES, Lui AJ, et al. Disrupting interferon-alpha and NF-kappaB crosstalk suppresses IFITM1 expression attenuating triple-negative breast cancer progression. Cancer Lett. 2021;514:12–29. doi:10.1016/j.canlet.2021.05.006
   PubMed Web of Science ®Google Scholar
• Suvannasankha A, Crean CD, Shanmugam R, et al. Antimyeloma effects of a sesquiterpene lactone parthenolide. Clin Cancer Res. 2008;14(6):1814–1822. doi:10.1158/1078-0432.CCR-07-1359
   PubMed Web of Science ®Google Scholar
• Jeyamohan S, Moorthy RK, Kannan MK, Arockiam AJ. Parthenolide induces apoptosis and autophagy through the suppression of PI3K/Akt signaling pathway in cervical cancer. Biotechnol Lett. 2016;38(8):1251–1260. doi:10.1007/s10529-016-2102-7
   PubMed Web of Science ®Google Scholar
• Sun J, Zhang C, Bao YL, et al. Parthenolide-induced apoptosis, autophagy and suppression of proliferation in HepG2 cells. Asian Pac J Cancer Prev. 2014;15(12):4897–4902. doi:10.7314/APJCP.2014.15.12.4897
   PubMedGoogle Scholar
• Pozarowski P, Halicka DH, Darzynkiewicz Z. Cell cycle effects and caspase-dependent and independent death of HL-60 and Jurkat cells treated with the inhibitor of NF-kappaB parthenolide. Cell Cycle. 2003;2(4):377–383. doi:10.4161/cc.2.4.420
   PubMed Web of Science ®Google Scholar
• Liu W, Wang X, Sun J, Yang Y, Li W, Song J. Parthenolide suppresses pancreatic cell growth by autophagy-mediated apoptosis. Onco Targets Ther. 2017;10:453–461. doi:10.2147/OTT.S117250
   PubMed Web of Science ®Google Scholar
• Lu C, Wang W, Jia Y, Liu X, Tong Z, Li B. Inhibition of AMPK/autophagy potentiates parthenolide-induced apoptosis in human breast cancer cells. J Cell Biochem. 2014;115(8):1458–1466. doi:10.1002/jcb.24808
   PubMed Web of Science ®Google Scholar
• Liu M, Yang Y, Liu D, Cao Y, Li Y. Parthenolide increases the sensitivity of gastric cancer cells to chemotherapy. J Tradit Chin Med. 2020;40(6):908–916. doi:10.19852/j.cnki.jtcm.2020.06.002
   PubMed Web of Science ®Google Scholar
• Tian B, Xiao Y, Ma J, et al. Parthenolide inhibits angiogenesis in esophageal squamous cell carcinoma through suppression of VEGF. Onco Targets Ther. 2020;13:7447–7458. doi:10.2147/OTT.S256291
   PubMed Web of Science ®Google Scholar
• Liu D, Han Y, Liu L, et al. Parthenolide inhibits the tumor characteristics of renal cell carcinoma. Int J Oncol. 2021;58(1):100–110. doi:10.3892/ijo.2020.5148
   PubMed Web of Science ®Google Scholar
• Zhu SM, Park YR, Seo SY, Kim IH, Lee ST, Kim SW. Parthenolide inhibits transforming growth factor beta1-induced epithelial-mesenchymal transition in colorectal cancer cells. Intest Res. 2019;17(4):527–536. doi:10.5217/ir.2019.00031
   PubMed Web of Science ®Google Scholar
• Iida-Norita R, Kawamura M, Suzuki Y, et al. Vasohibin-2 plays an essential role in metastasis of pancreatic ductal adenocarcinoma. Cancer Sci. 2019;110(7):2296–2308. doi:10.1111/cas.14041
   PubMed Web of Science ®Google Scholar
• Wu SY, Xing F, Sharma S, et al. Nicotine promotes brain metastasis by polarizing microglia and suppressing innate immune function. J Exp Med. 2020;217(8). doi:10.1084/jem.20191131
   Web of Science ®Google Scholar
• Jin X, Yang Q, Cai N, Zhang Z. A cocktail of betulinic acid, parthenolide, honokiol and ginsenoside Rh2 in liposome systems for lung cancer treatment. Nanomedicine. 2020;15(1):41–54. doi:10.2217/nnm-2018-0479
   PubMed Web of Science ®Google Scholar
• Jin X, Lu X, Zhang Z, Lv H. Indocyanine green-parthenolide thermosensitive liposome combination treatment for triple-negative breast cancer. Int J Nanomedicine. 2020;15:3193–3206. doi:10.2147/IJN.S245289
   PubMed Web of Science ®Google Scholar
• Gao W, Li L, Zhang X, et al. Nanomagnetic liposome-encapsulated parthenolide and indocyanine green for targeting and chemo-photothermal antitumor therapy. Nanomedicine. 2020;15(9):871–890. doi:10.2217/nnm-2019-0038
   PubMed Web of Science ®Google Scholar
• Jin X, Zhou J, Zhang Z, Lv H. The combined administration of parthenolide and ginsenoside CK in long circulation liposomes with targeted tLyp-1 ligand induce mitochondria-mediated lung cancer apoptosis. Artif Cells Nanomed Biotechnol. 2018;46(sup3):S931–S942. doi:10.1080/21691401.2018.1518913
   PubMed Web of Science ®Google Scholar
• Gao W, Wei S, Li Z, et al. Nano magnetic liposomes-encapsulated parthenolide and glucose oxidase for ultra-efficient synergistic antitumor therapy. Nanotechnology. 2020;31(35):355104. doi:10.1088/1361-6528/ab92c8
   PubMed Web of Science ®Google Scholar
• Liu Y, Lu WL, Guo J, et al. A potential target associated with both cancer and cancer stem cells: a combination therapy for eradication of breast cancer using vinorelbine stealthy liposomes plus parthenolide stealthy liposomes. J Control Release. 2008;129(1):18–25. doi:10.1016/j.jconrel.2008.03.022
   PubMed Web of Science ®Google Scholar
• Baranello MP, Bauer L, Benoit DS. Poly(styrene-alt-maleic anhydride)-based diblock copolymer micelles exhibit versatile hydrophobic drug loading, drug-dependent release, and internalization by multidrug resistant ovarian cancer cells. Biomacromolecules. 2014;15(7):2629–2641. doi:10.1021/bm500468d
   PubMed Web of Science ®Google Scholar
• Baranello MP, Bauer L, Jordan CT, Benoit DSW. Micelle delivery of parthenolide to acute myeloid leukemia cells. Cell Mol Bioeng. 2015;8(3):455–470. doi:10.1007/s12195-015-0391-x
   PubMed Web of Science ®Google Scholar
• Ridolfo R, Ede BC, Diamanti P, et al. Biodegradable, drug-loaded nanovectors via direct hydration as a new platform for cancer therapeutics. Small. 2018;14(32):e1703774. doi:10.1002/smll.201703774
   PubMed Web of Science ®Google Scholar
• Deller RC, Diamanti P, Morrison G, et al. Functionalized triblock copolymer vectors for the treatment of acute lymphoblastic leukemia. Mol Pharm. 2017;14(3):722–732. doi:10.1021/acs.molpharmaceut.6b01008
   PubMedGoogle Scholar
• Gill KK, Kaddoumi A, Nazzal S. Mixed micelles of PEG(2000)-DSPE and vitamin-E TPGS for concurrent delivery of paclitaxel and parthenolide: enhanced chemosenstization and antitumor efficacy against non-small cell lung cancer (NSCLC) cell lines. Eur j Pharm Sci. 2012;46(1–2):64–71. doi:10.1016/j.ejps.2012.02.010
   PubMed Web of Science ®Google Scholar
• Zong H, Sen S, Zhang G, et al. In vivo targeting of leukemia stem cells by directing parthenolide-loaded nanoparticles to the bone marrow niche. Leukemia. 2016;30(7):1582–1586. doi:10.1038/leu.2015.343
   PubMed Web of Science ®Google Scholar
• Ran D, Zhou J, Chai Z, et al. All-stage precisional glioma targeted therapy enabled by a well-designed D-peptide. Theranostics. 2020;10(9):4073–4087. doi:10.7150/thno.41382
   PubMed Web of Science ®Google Scholar
• Liang P, Wu H, Zhang Z, Jiang S, Lv H. Preparation and characterization of parthenolide nanocrystals for enhancing therapeutic effects of sorafenib against advanced hepatocellular carcinoma. Int J Pharm. 2020;583:119375. doi:10.1016/j.ijpharm.2020.119375
   PubMedGoogle Scholar
• Darwish NHE, Sudha T, Godugu K, et al. Novel targeted nano-parthenolide molecule against NF-kB in acute myeloid leukemia. Molecules. 2019;24(11):2103. doi:10.3390/molecules24112103
   PubMed Web of Science ®Google Scholar
• Karmakar A, Xu Y, Mustafa T, et al. Nanodelivery of parthenolide using functionalized nanographene enhances its anticancer activity. Rsc Adv. 2015;5(4):2411–2420. doi:10.1039/C4RA10871J
   PubMed Web of Science ®Google Scholar
• Collnot EM, Baldes C, Schaefer UF, et al. TPGS P-glycoprotein inhibition mechanism: influence on conformational flexibility, intracellular ATP levels, and role of time and site of access. Mol Pharm. 2010;7(3):642–651. doi:10.1021/mp900191s
   PubMed Web of Science ®Google Scholar
• Legras S, Gunthert U, Stauder R, et al. A strong expression of CD44-6v correlates with shorter survival of patients with acute myeloid leukemia. Blood. 1998;91(9):3401–3413. doi:10.1182/blood.V91.9.3401
   PubMed Web of Science ®Google Scholar
• Sun D, Zhou JK, Zhao L, et al. Novel curcumin liposome modified with hyaluronan targeting CD44 plays an anti-leukemic role in acute myeloid leukemia in vitro and in vivo. ACS Appl Mater Interfaces. 2017;9(20):16857–16868. doi:10.1021/acsami.7b02863
   PubMed Web of Science ®Google Scholar
• Wang W, Li M, Zhang Z, et al. Design, synthesis and evaluation of multi-functional tLyP-1-hyaluronic acid-paclitaxel conjugate endowed with broad anticancer scope. Carbohydr Polym. 2017;156:97–107. doi:10.1016/j.carbpol.2016.08.100
   PubMed Web of Science ®Google Scholar
• Viennois E, Xiao B, Ayyadurai S, et al. Micheliolide, a new sesquiterpene lactone that inhibits intestinal inflammation and colitis-associated cancer. Lab Invest. 2014;94(9):950–965. doi:10.1038/labinvest.2014.89
   PubMed Web of Science ®Google Scholar
• Penthala NR, Balasubramaniam M, Dachavaram SS, et al. Antitumor properties of novel sesquiterpene lactone analogs as NFkappaB inhibitors that bind to the IKKbeta ubiquitin-like domain (ULD). Eur J Med Chem. 2021;224:113675. doi:10.1016/j.ejmech.2021.113675
   PubMed Web of Science ®Google Scholar
• Huang H, Park S, Zhang H, et al. Targeting AKT with costunolide suppresses the growth of colorectal cancer cells and induces apoptosis in vitro and in vivo. J Exp Clin Cancer Res. 2021;40(1):114. doi:10.1186/s13046-021-01895-w
   PubMed Web of Science ®Google Scholar
• Zeng B, Cheng Y, Zheng K, et al. Design, synthesis and in vivo anticancer activity of novel parthenolide and micheliolide derivatives as NF-kappaB and STAT3 inhibitors. Bioorg Chem. 2021;111:104973. doi:10.1016/j.bioorg.2021.104973
   PubMed Web of Science ®Google Scholar
• Ma WW, Shi QQ, Ding YH, Long J, Zhang Q, Chen Y. Synthesis of micheliolide derivatives and their activities against AML progenitor cells. Molecules. 2013;18(5):5980–5992. doi:10.3390/molecules18055980
   PubMed Web of Science ®Google Scholar
• Ding Y, Guo H, Ge W, et al. Copper(I) oxide nanoparticles catalyzed click chemistry based synthesis of melampomagnolide B-triazole conjugates and their anti-cancer activities. Eur J Med Chem. 2018;156:216–229. doi:10.1016/j.ejmech.2018.06.058
   PubMed Web of Science ®Google Scholar
• Janganati V, Ponder J, Thakkar S, Jordan CT, Crooks PA. Succinamide derivatives of melampomagnolide B and their anti-cancer activities. Bioorg Med Chem. 2017;25(14):3694–3705. doi:10.1016/j.bmc.2017.05.008
   PubMed Web of Science ®Google Scholar
• Srivastava SK, Abraham A, Bhat B, et al. Synthesis of 13-amino costunolide derivatives as anticancer agents. Bioorg Med Chem Lett. 2006;16(16):4195–4199. doi:10.1016/j.bmcl.2006.05.083
   PubMed Web of Science ®Google Scholar
• Ackun-Farmmer MA, Alwaseem H, Counts M, et al. Nanoparticle-mediated delivery of micheliolide analogs to eliminate leukemic stem cells in the bone marrow. Adv Ther. 2022;5(1). doi:10.1002/adtp.202100100
   Web of Science ®Google Scholar
• El-Far AH, Godugu K, Salaheldin TA, Darwish NHE, Saddiq AA, Mousa SA. Nanonutraceuticals: anti-cancer activity and improved safety of chemotherapy by costunolide and its nanoformulation against colon and breast cancer. Biomedicines. 2021;9(8):990. doi:10.3390/biomedicines9080990
   PubMed Web of Science ®Google Scholar
• Niu X, Wang X, Niu B, et al. Costunolide loaded in pH-responsive mesoporous silica nanoparticles for increased stability and an enhanced anti-fibrotic effect. Pharmaceuticals. 2021;14(10):951. doi:10.3390/ph14100951
   Web of Science ®Google Scholar
• Caruthers SD, Wickline SA, Lanza GM. Nanotechnological applications in medicine. Curr Opin Biotechnol. 2007;18(1):26–30. doi:10.1016/j.copbio.2007.01.006
   PubMed Web of Science ®Google Scholar
• Khan H, Ullah H, Martorell M, et al. Flavonoids nanoparticles in cancer: treatment, prevention and clinical prospects. Semin Cancer Biol. 2021;69:200–211. doi:10.1016/j.semcancer.2019.07.023
   PubMed Web of Science ®Google Scholar
• Rahaiee S, Assadpour E, Faridi Esfanjani A, Silva AS, Jafari SM. Application of nano/microencapsulated phenolic compounds against cancer. Adv Colloid Interface Sci. 2020;279:102153. doi:10.1016/j.cis.2020.102153
   PubMed Web of Science ®Google Scholar
• Paul S, Roy D, Pati S, Sa G. The adroitness of andrographolide as a natural weapon against colorectal cancer. Front Pharmacol. 2021;12:731492. doi:10.3389/fphar.2021.731492
   PubMed Web of Science ®Google Scholar
• Schuldt M, Pei J, Harakalova M, et al. Proteomic and functional studies reveal detyrosinated tubulin as treatment target in sarcomere mutation-induced hypertrophic cardiomyopathy. Circ Heart Fail. 2021;14(1):e007022. doi:10.1161/CIRCHEARTFAILURE.120.007022
   PubMed Web of Science ®Google Scholar
• Wang D, Liu S, Xu S. Identification of hub genes, key pathways, and therapeutic agents in Hutchinson-Gilford Progeria syndrome using bioinformatics analysis. Medicine. 2020;99(7):e19022. doi:10.1097/MD.0000000000019022
   PubMed Web of Science ®Google Scholar