165
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Tarin-Loaded Nanoliposomes Activate Apoptosis and Autophagy and Inhibit the Migration of Human Mammary Adenocarcinoma Cells

, ORCID Icon, , , , ORCID Icon, , ORCID Icon & ORCID Icon show all
Pages 6393-6408 | Received 09 Sep 2023, Accepted 28 Oct 2023, Published online: 06 Nov 2023

References

  • Antoniou AI, Giofrè S, Seneci P, Passarella D, Pellegrino S. Stimulus-responsive liposomes for biomedical applications. Drug Discov Today. 2021;26(8):1794–1824. doi:10.1016/j.drudis.2021.05.010
  • Al-Mahmood S, Sapiezynski J, Garbuzenko OB, Minko T. Metastatic and triple-negative breast cancer: challenges and treatment options. Drug Deliv Transl Res. 2018;8:1483–1507. doi:10.1007/s13346-018-0551-3
  • Waks AG, Winer EP. Breast cancer treatment: a review. JAMA. 2019;321(3):288–300. doi:10.1001/jama.2018.19323
  • Sharifi M, Jafari S, Hasan A, et al. Antimetastatic activity of lactoferrin-coated mesoporous maghemite nanoparticles in breast cancer enabled by combination therapy. ACS Biomater Sci Eng. 2020;6(6):3574–3584. doi:10.1021/acsbiomaterials.0c00086
  • ElOuassif B, Idri A, Hosni M, Abran A. Classification techniques in breast cancer diagnosis: a systematic literature review. Comput Methods Biomech Biomed Eng Imaging Vis. 2021;9(1):50–77.
  • Vahed SZ, Salehi R, Davaran S, Sharifi S. Liposome-based drug co-delivery systems in cancer cells. Mater Sci Eng C. 2017;71:1327–1341. doi:10.1016/j.msec.2016.11.073
  • Zuris JA, Thompson DB, Shu Y, et al. Cationic lipid-mediated delivery of proteins enables efficient protein-based genome editing in vitro and in vivo. Nat Biotechnol. 2015;33(1):73–80. doi:10.1038/nbt.3081
  • Wang M, Zuris JA, Meng F, et al. Efficient delivery of genome-editing proteins using bioreducible lipid nanoparticles. Proc Natl Acad Sci. 2016;113(11):2868–2873. doi:10.1073/pnas.1520244113
  • Chen W, Deng W, Goldys EM. Light-triggerable liposomes for enhanced endolysosomal escape and gene silencing in PC12 cells. Mol Ther Nucleic Acids. 2017;7:366–377. doi:10.1016/j.omtn.2017.04.015
  • Xiao H, Li C, Dai Y, Cheng Z, Hou Z, Lin J. Inorganic nanocarriers for platinum drug delivery. Mater Today. 2015;18(10):554–564. doi:10.1016/j.mattod.2015.05.017
  • Pattni BS, Chupin VV, Torchilin VP. New developments in liposomal drug delivery. Chem Rev. 2015;115(19):10938–10966. doi:10.1021/acs.chemrev.5b00046
  • Zylberberg C, Gaskill K, Pasley S, Matosevic S. Engineering liposomal nanoparticles for targeted gene therapy. Gene Ther. 2017;24(8):441–452. doi:10.1038/gt.2017.41
  • Weis SM, Cheresh DA. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat Med. 2011;17(11):1359–1370. doi:10.1038/nm.2537
  • Woodle M, Collins L, Sponsler E, Kossovsky N, Papahadjopoulos D, Martin F. Sterically stabilized liposomes. Reduction in electrophoretic mobility but not electrostatic surface potential. Biophys J. 1992;61(4):902–910. doi:10.1016/S0006-3495(92)81897-0
  • Zhao M, Ding X-F, Shen J-Y, Zhang X-P, Ding X-W, Xu B. Use of liposomal doxorubicin for adjuvant chemotherapy of breast cancer in clinical practice. J Zhejiang Univ Sci B. 2017;18(1):15. doi:10.1631/jzus.B1600303
  • Din F, Aman W, Ullah I, et al. Effective use of nanocarriers as drug delivery systems for the treatment of selected tumors. Int J Nanomedicine. 2017;12:7291–7309. doi:10.2147/IJN.S146315
  • Dong M, Luo L, Ying X, et al. Comparable efficacy and less toxicity of pegylated liposomal doxorubicin versus epirubicin for neoadjuvant chemotherapy of breast cancer: a case-control study. Onco Targets Ther. 2018;11:4247–4252. doi:10.2147/OTT.S162003
  • Gabizon AA, Patil Y, La-Beck NM. New insights and evolving role of pegylated liposomal doxorubicin in cancer therapy. Drug Resist Updat. 2016;29:90–106. doi:10.1016/j.drup.2016.10.003
  • Haddadzadegan S, Dorkoosh F, Bernkop-Schnürch A. Oral delivery of therapeutic peptides and proteins: technology landscape of lipid-based nanocarriers. Adv Drug Deliv Rev. 2022;182:114097. doi:10.1016/j.addr.2021.114097
  • Jain D, Mahammad SS, Singh PP, Kodipyaka R. A review on parenteral delivery of peptides and proteins. Drug Dev Ind Pharm. 2019;45(9):1403–1420. doi:10.1080/03639045.2019.1628770
  • Bruno BJ, Miller GD, Lim CS. Basics and recent advances in peptide and protein drug delivery. Ther Deliv. 2013;4(11):1443–1467. doi:10.4155/tde.13.104
  • Pereira PR, Del Aguila EM, Verícimo MA, Zingali RB, Paschoalin VMF, Silva JT. Purification and characterization of the lectin from taro (Colocasia esculenta) and its effect on mouse splenocyte proliferation in vitro and in vivo. Protein J. 2014;33:92–99. doi:10.1007/s10930-013-9541-y
  • Pereira PR, Winter HC, Verícimo MA, et al. Structural analysis and binding properties of isoforms of tarin, the GNA-related lectin from Colocasia esculenta. Biochim Biophys Acta. 2015;1854(1):20–30. doi:10.1016/j.bbapap.2014.10.013
  • Pereira PR, Silva JT, Verícimo MA, Paschoalin VM, Teixeira GA. Crude extract from taro (Colocasia esculenta) as a natural source of bioactive proteins able to stimulate haematopoietic cells in two murine models. J Funct Foods. 2015;18:333–343. doi:10.1016/j.jff.2015.07.014
  • Pereira PR, Meagher JL, Winter HC, et al. High-resolution crystal structures of Colocasia esculenta tarin lectin. Glycobiology. 2017;27(1):50–56. doi:10.1093/glycob/cww083
  • Sang Chan Y, Ho Wong J, Bun Ng T. A cytokine-inducing hemagglutinin from small taros. Protein Pept Lett. 2010;17(7):823–830. doi:10.2174/092986610791306742
  • Kundu N, Campbell P, Hampton B, et al. Antimetastatic activity isolated from Colocasia esculenta (taro). Anticancer Drugs. 2012;23(2):200–211. doi:10.1097/CAD.0b013e32834b85e8
  • Pereira PR, Corrêa ACNTF, Vericimo MA, Paschoalin VMF. Tarin, a potential immunomodulator and COX‐inhibitor lectin found in taro (Colocasia esculenta). Compr Rev Food Sci Food Saf. 2018;17(4):878–891. doi:10.1111/1541-4337.12358
  • Mérida LA, Mattos ÉB, Corrêa AC, et al. Tarin stimulates granulocyte growth in bone marrow cell cultures and minimizes immunosuppression by cyclo-phosphamide in mice. PLoS One. 2018;13(11):e0206240. doi:10.1371/journal.pone.0206240
  • Wu L, Bao J-K. Anti-tumor and anti-viral activities of Galanthus nivalis agglutinin (GNA)-related lectins. Glycoconj J. 2013;30:269–279. doi:10.1007/s10719-012-9440-z
  • Corrêa AC, Vericimo MA, Dashevskiy A, Pereira PR, Paschoalin VM. Liposomal taro lectin nanocapsules control human glioblastoma and mammary adenocarcinoma cell proliferation. Molecules. 2019;24(3):471. doi:10.3390/molecules24030471
  • Corrêa AC, Pereira PR, Paschoalin VM. Preparation and characterization of nanoliposomes for the entrapment of bioactive hydrophilic globular proteins. JoVE. 2019;150:e59900.
  • Kundu N, Ma X, Hoag S, et al. An extract of taro (Colocasia esculenta) mediates potent inhibitory actions on metastatic and cancer stem cells by tumor cell-autonomous and immune-dependent mechanisms. Breast Cancer. 2021;15:11782234211034937. doi:10.1177/11782234211034937
  • Yasin U, Bilal M, Bashir H, Amirzada MI, Sumrin A, Asad MHHB. Preparation and nanoencapsulation of lectin from Lepidium sativum on chitosan-tripolyphosphate nanoparticle and their cytotoxicity against hepatocellular carcinoma cells (HepG2). Biomed Res Int. 2020;2020:1–11. doi:10.1155/2020/7251346
  • Roy A, Banerjee S, Majumder P, Das S. Efficiency of mannose-binding plant lectins in controlling a homopteran insect, the red cotton bug. J Agric Food Chem. 2002;50(23):6775–6779. doi:10.1021/jf025660x
  • Dos Santos Ferreira D, Faria SD, de Araújo Lopes SC, et al. Development of a bone-targeted pH-sensitive liposomal formulation containing doxorubicin: physicochemical characterization, cytotoxicity, and biodistribution evaluation in a mouse model of bone metastasis. Int J Nanomedicine. 2016;11:3737. doi:10.2147/IJN.S109966
  • McMillian M, Li L, Parker J, et al. An improved resazurin-based cytotoxicity assay for hepatic cells. Cell Biol Toxicol. 2002;18:157–173. doi:10.1023/A:1015559603643
  • Grada A, Otero-Vinas M, Prieto-Castrillo F, Obagi Z, Falanga V. Research techniques made simple: analysis of collective cell migration using the wound healing assay. J Invest Dermatol. 2017;137(2):e11–e16. doi:10.1016/j.jid.2016.11.020
  • Diniz Filho JFS, de Barros A, Pijeira MSO, et al. Ultrastructural analysis of cancer cells treated with the radiopharmaceutical radium dichloride ([223Ra]RaCl2): understanding the effect on cell structure. Cells. 2023;12(3):451. doi:10.3390/cells12030451
  • Filippi-Chiela EC, Villodre ES, Zamin LL, Lenz G. Autophagy interplay with apoptosis and cell cycle regulation in the growth inhibiting effect of resveratrol in glioma cells. PLoS One. 2011;6(6):e20849. doi:10.1371/journal.pone.0020849
  • Jiang H, White EJ, Conrad C, Gomez-Manzano C, Fueyo J. Autophagy pathways in glioblastoma. Methods Enzymol. 2009;453:273–286.
  • Hu Z-Y, Sun J, Zhu X-F, Yang D, Zeng Y-X. ApoG2 induces cell cycle arrest of nasopharyngeal carcinoma cells by suppressing the c-Myc signaling pathway. J Transl Med. 2009;7:1–11. doi:10.1186/1479-5876-7-74
  • Maruyama K. Intracellular targeting delivery of liposomal drugs to solid tumors based on EPR effects. Adv Drug Deliv Rev. 2011;63(3):161–169. doi:10.1016/j.addr.2010.09.003
  • Milla P, Dosio F, Cattel L. PEGylation of proteins and liposomes: a powerful and flexible strategy to improve the drug delivery. Curr Drug Metab. 2012;13(1):105–119. doi:10.2174/138920012798356934
  • Shiraishi K, Yokoyama M. Toxicity and immunogenicity concerns related to PEGylated-micelle carrier systems: a review. Sci Technol Adv Mater. 2019;20(1):324–336. doi:10.1080/14686996.2019.1590126
  • Ishida T, Ichihara M, Wang X, Kiwada H. Spleen plays an important role in the induction of accelerated blood clearance of PEGylated liposomes. J Control Release. 2006;115(3):243–250. doi:10.1016/j.jconrel.2006.08.001
  • Wu J-S, Jiang J, Chen B-J, Wang K, Tang Y-L, Liang X-H. Plasticity of cancer cell invasion: patterns and mechanisms. Transl Oncol. 2021;14(1):100899. doi:10.1016/j.tranon.2020.100899
  • Gupta GP, Massagué J. Cancer metastasis: building a framework. Cell. 2006;127(4):679–695. doi:10.1016/j.cell.2006.11.001
  • Fares J, Fares MY, Khachfe HH, Salhab HA, Fares Y. Molecular principles of metastasis: a hallmark of cancer revisited. Signal Transduct Target Ther. 2020;5(1):28. doi:10.1038/s41392-020-0134-x
  • Liu Z, Luo Y, Zhou -T-T, Zhang W-Z. Could plant lectins become promising anti-tumour drugs for causing autophagic cell death? Cell Prolif. 2013;46(5):509–515. doi:10.1111/cpr.12054
  • Mazalovska M, Kouokam JC. Plant-derived lectins as potential cancer therapeutics and diagnostic tools. Biomed Res Int. 2020;2020:1631394. doi:10.1155/2020/1631394
  • Li C-Y, Meng L, Liu B, Bao J-K. Galanthus nivalis agglutinin (GNA)-related lectins: traditional proteins, burgeoning drugs? Curr Chem Biol. 2009;3(3):323–333. doi:10.2174/187231309789054913
  • Ribeiro Pereira P, Bertozzi de Aquino Mattos É, Nitzsche Teixeira Fernandes Correa AC, Afonso Vericimo M, Margaret Flosi Paschoalin V. Anticancer and Immunomodulatory Benefits of Taro (Colocasia esculenta) Corms, an underexploited tuber crop. Int J Mol Sci. 2020;22(1):265. doi:10.3390/ijms22010265
  • Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010;140(3):313–326. doi:10.1016/j.cell.2010.01.028
  • Yau T, Dan X, Ng CCW, Ng TB. Lectins with potential for anti-cancer therapy. Molecules. 2015;20(3):3791–3810. doi:10.3390/molecules20033791
  • Bhutia SK, Panda PK, Sinha N, et al. Plant lectins in cancer therapeutics: targeting apoptosis and autophagy-dependent cell death. Pharmacol Res. 2019;144:8–18. doi:10.1016/j.phrs.2019.04.001
  • Xi H, Wang S, Wang B, et al. The role of interaction between autophagy and apoptosis in tumorigenesis (Review). Oncol Rep. 2022;48(6):208. doi:10.3892/or.2022.8423
  • Das S, Shukla N, Singh SS, Kushwaha S, Shrivastava R. Mechanism of interaction between autophagy and apoptosis in cancer. Apoptosis. 2021;26(9):512–533. doi:10.1007/s10495-021-01687-9
  • Xie Q, Liu Y, Li X. The interaction mechanism between autophagy and apoptosis in colon cancer. Transl Oncol. 2020;13(12):100871. doi:10.1016/j.tranon.2020.100871
  • Su M, Mei Y, Sinha S. Role of the crosstalk between autophagy and apoptosis in cancer. J Oncol. 2013;2013:102735. doi:10.1155/2013/102735
  • Wang S-Y, Yu Q-J, Bao J-K, Liu B. Polygonatum cyrtonema lectin, a potential antineoplastic drug targeting programmed cell death pathways. Biochem Biophys Res Commun. 2011;406(4):497–500. doi:10.1016/j.bbrc.2011.02.049
  • Ouyang L, Chen Y, Wang X-Y, et al. Polygonatum odoratum lectin induces apoptosis and autophagy via targeting EGFR-mediated Ras-Raf-MEK-ERK pathway in human MCF-7 breast cancer cells. Phytomedicine. 2014;21(12):1658–1665. doi:10.1016/j.phymed.2014.08.002
  • Liu B, Cheng Y, Zhang B, Bian H-J, Bao J-K. Polygonatum cyrtonema lectin induces apoptosis and autophagy in human melanoma A375 cells through a mitochondria-mediated ROS–p38–p53 pathway. Cancer Lett. 2009;275(1):54–60. doi:10.1016/j.canlet.2008.09.042
  • Liu T, Wu L, Wang D, et al. Role of reactive oxygen species-mediated MAPK and NF-κB activation in polygonatum cyrtonema lectin-induced apoptosis and autophagy in human lung adenocarcinoma A549 cells. J Biochem. 2016;160(6):315–324. doi:10.1093/jb/mvw040
  • Wu L, Liu T, Xiao Y, et al. Polygonatum odoratum lectin induces apoptosis and autophagy by regulation of microRNA-1290 and microRNA-15a-3p in human lung adenocarcinoma A549 cells. Int J Biol Macromol. 2016;85:217–226. doi:10.1016/j.ijbiomac.2015.11.014
  • Tsapras P, Nezis IP. Caspase involvement in autophagy. Cell Death Differ. 2017;24(8):1369–1379. doi:10.1038/cdd.2017.43