615
Views
23
CrossRef citations to date
0
Altmetric
Review

Pleiotropic Anticancer Properties of Scorpion Venom Peptides: Rhopalurus princeps Venom as an Anticancer Agent

, ORCID Icon, , , , & show all
Pages 881-893 | Published online: 27 Feb 2020

References

  • Cancer Research UK. Available from: https://www.cancerresearchuk.org/. Assessed 14 February, 2020.
  • BalwitJM, HwuP, UrbaWJ, MarincolaFM. The iSBTc/SITC primer on tumor immunology and biological therapy of cancer: a summary of the 2010 program. J Transl Med. 2011;9:18. doi:10.1186/1479-5876-9-1821281484
  • AlshakerHA, MatalkaKZ. IFN-γ, IL-17 and TGF-β involvement in shaping the tumor microenvironment: the significance of modulating such cytokines in treating malignant solid tumors. Cancer Cell Int. 2011;11:33. doi:10.1186/1475-2867-11-3321943203
  • LitanA, LanghansSA. Cancer as a channelopathy: ion channels and pumps in tumor development and progression. Front Cell Neurosci. 2015;9:86. doi:10.3389/fncel.2015.0008625852478
  • MarshallHT, DjamgozMBA. Immuno-oncology: emerging targets and combination therapies. Front Oncol. 2018;8:315. doi:10.3389/fonc.2018.0031530191140
  • PoornimaP, KumarJD, ZhaoQ, BlunderM, EfferthT. Net-work pharmacology of cancer: from understanding of complex interactomes to the design of multi-target specific therapeutics from nature. Pharmacol Res. 2016;111:290–302. doi:10.1016/j.phrs.2016.06.01827329331
  • McferrinMB, SontheimerH. A role for ion channels in glioma cell invasion. Neuron Glia Biol. 2006;2(1):39–49. doi:10.1017/S1740925X0600004416520829
  • SontheimerH. An unexpected role for ion channels in brain tumor metastasis. Exp Biol Med. 2008;233:779–791. doi:10.3181/0711-MR-308
  • BustinSA, LiSR, DorudiS. Expression of the Ca2C-activated chloride channel genes CLCA1 and CLCA2 is downregulated in human colorectal cancer. DNA Cell Biol. 2001;20:331–338. doi:10.1089/1044549015212244211445004
  • UllrichN, SontheimerH. Cell cycle-dependent expression of a glioma-specific chloride current: proposed link to cytoskeletal changes. Am J Physiol. 1997;273:C1290–C1297. doi:10.1152/ajpcell.1997.273.4.C12909357773
  • TurnerKL, SontheimerH. Cl− and K+ channels and their role in primary brain tumour biology. Philos Trans R Soc Lond B Biol Sci. 2014;369:20130095. doi:10.1098/rstb.2013.009524493743
  • LiuYF, HuJ, ZhangJH, WangSL, WuCF. Isolation purification, and N terminal partial sequence of an anti-tumor-analgesic peptide from the venom of the Chinese scorpion Buthus martensii Karsch. Prep Biochem Biotechnol. 2002;32:317–327. doi:10.1081/PB-12001545612455825
  • NorthcottPA, DubucAM, PfisterS, TaylorMD. Molecular subgroups of medulloblastoma. Expert Rev Neurother. 2012;12:871–884. doi:10.1586/ern.12.6622853794
  • ComesN, BielanskaJ, Vallejo-GraciaA, et al. The voltage-dependent K.C/channels KV1.3 and KV1.5 in human cancer. Front Physiol. 2013;4:283. doi:10.3389/fphys.2013.0028324133455
  • ComesN, Serrano-AlbarrásA, CaperaJ, et al. Involvement of potassium channels in the progression of cancer to a more malignant phenotype. Biochim Biophys Acta. 2015;1848(10 Pt B):2477–2492. doi:10.1016/j.bbamem.2014.12.00825517985
  • ChioniAM, ShaoD, GroseR, DjamgozMB. Protein kinase A and regulation of neonatal NaV1.5 expression in human breast cancer cells: activity-dependent positive feedback and cellular migration. Int J Biochem Cell Biol. 2010;42:346–358. doi:10.1016/j.biocel.2009.11.02119948241
  • BrissonL, DriffortV, BenoistL, et al. NaV1.5 NaC channels allosterically regulate the NHE-1 exchanger and promote the activity of breast cancer cell invadopodia. J Cell Sci. 2013;126:4835–4842. doi:10.1242/jcs.12390123902689
  • DriffortV, GilletL, BonE, et al. Ranolazine inhibits NaV1.5-mediated breast cancer cell invasiveness and lung colonization. Mol Cancer. 2014;13:264. doi:10.1186/1476-4598-13-26425496128
  • XingD, WangJ, OuS, et al. Expression of neonatal NaV1.5 in human brain astrocytoma and its effect on proliferation, invasion and apoptosis of astrocytoma cells. Oncol Rep. 2014;31:2692–2700. doi:10.3892/or.2014.314324756536
  • FraserSP, Ozerlat-GunduzI, BrackenburyWJ, et al. Regulation of voltage-gated sodium channel expression in cancer: hormones, growth factors and auto-regulation. Philos Trans R Soc Lond B Biol Sci. 2014;369:20130105. doi:10.1098/rstb.2013.010524493753
  • AydarE, YeoS, DjamgozM, PalmerC. Abnormal expression, localization and interaction of canonical transient receptor potential ion channels in human breast cancer cell lines and tissues: a potential target for breast cancer diagnosis and therapy. Cancer Cell Int. 2009;9:23. doi:10.1186/1475-2867-9-2319689790
  • DingX, HeZ, ZhouK, et al. Essential role of TRPC6 channels in G2/M phase transition and development of human glioma. J Natl Cancer Inst. 2010;102:1052–1068. doi:10.1093/jnci/djq21720554944
  • ZhangY, WangH, QianZ, et al. Low voltage- activated T-type Ca2C channel inhibitors as new tools in the treatment of glioblastoma: the role of endostatin. Pflugers Arch. 2014;466:811–818. doi:10.1007/s00424-013-1427-524407946
  • Quintero-HernándezV, Jiménez-VargasJM, GurrolaGB, ValdiviaHH, PossaniLD. Scorpion venom components that affect ion-channels function. Toxicon. 2013;76:328–342. doi:10.1016/j.toxicon.2013.07.01223891887
  • Díaz-GarcíaA, Morier-DíazL, Frión-HerreraY, et al. In vitro anticancer effect of venom from cuban scorpion Rhopalurus junceus against a panel of human cancer cell lines. J Venom Res. 2013;4:5–12.23946884
  • ZarganJ, UmarS, SajadM, et al. Scorpion venom (Odontobuthus doriae) induces apoptosis by depolarization of mitochondria and reduces S-phase population in human breast cancer cells (MCF-7). Toxicol in Vitro. 2011;25(8):1748–1756. doi:10.1016/j.tiv.2011.09.00221945044
  • ZarganJ, MirS, UmarS, et al. Scorpion (Odontobuthus doriae) venom induces apoptosis and inhibits DNA synthesis in human neuroblastoma cells. Mol Cell Biochem. 2010;348(1–2):173–181. doi:10.1007/s11010-010-0652-x
  • ZangYY, WuLC, WangZP, et al. Anti-proliferation effect of polypeptide extracted from scorpion venom on human prostate cancer cells in vitro. J Clin Med Res. 2009;1(1):24–31. doi:10.4021/jocmr2009.01.122022505961
  • Al-AsmariAK, RiyasdeenA, AbbasmanthiriR, ArshaduddinM, Al-HarthiFA. Scorpion (Androctonus bicolor) venom exhibits cytotoxicity and induces cell cycle arrest and apoptosis in breast and colorectal cancer cell lines. Indian J Pharmacol. 2016;48(5):537–543. doi:10.4103/0253-7613.19074227721540
  • Al-AsmariAK, RiyasdeenA, IslamM. Scorpion venom causes upregulation of p53 and downregulation of Bcl-xL and BID protein expression by modulating signaling proteins Erk1/2 and STAT3, and DNA damage in breast and colorectal cancer cell lines. Integr Cancer Ther. 2018;17(2):271–281. doi:10.1177/153473541770494928438053
  • Al-AsmariAK, IslamM, Al-ZahraniAM. In vitro analysis of the anticancer properties of scorpion venom in colorectal and breast cancer cell lines. Oncol Lett. 2016;11(2):1256–1262. doi:10.3892/ol.2015.403626893728
  • GuptaSD, GomesA, DebnathA, SahaA, GomesA. Apoptosis induction in human leukemic cells by a novel protein Bengalin, isolated from Indian black scorpion venom: through mitochondrial pathway and inhibition of heat shock proteins. Chem Biol Interact. 2010;183:293–303. doi:10.1016/j.cbi.2009.11.00619913524
  • D’SuzeG, RosalesA, SalazarV, SevcikC. Apoptogenic peptides from Tityus discrepans scorpion venom acting against the SKBR3 breast cancer cell line. Toxicon. 2010;56(8):1497–1505. doi:10.1016/j.toxicon.2010.09.00820888852
  • Al-AsmariAK, RiyasdeenA, IslamM. Scorpion venom causes apoptosis by increasing reactive oxygen species and cell cycle arrest in MDA-MB-231 and HCT-8 cancer cell lines. J Evid Based Integr Med. 2018;23:2156587217751796.29405760
  • ZarganJ, SajadM, UmarS, et al. Scorpion (Androctonus crassicauda) venom limits growth of transformed cells (SH-SY5Y and MCF-7) by cytotoxicity and cell cycle arrest. Exp Mol Pathol. 2011;91(1):447–454. doi:10.1016/j.yexmp.2011.04.00821536027
  • LiB, LyuP, XiX, et al. Triggering of cancer cell cycle arrest by a novel scorpion venom-derived peptide-Gonearrestide. J Cell Mol Med. 2018;22(9):4460–4473. doi:10.1111/jcmm.2018.22.issue-929993185
  • SalemML, ShoukryNM, TelebWK, Abdel-DaimMM, Abdel-RahmanMA. In vitro and in vivo antitumor effects of the Egyptian scorpion Androctonus amoreuxi venom in an Ehrlich ascites tumor model. Springer Plus. 2016;5:570. doi:10.1186/s40064-016-2269-327247867
  • Al AsmariAK, KhanAQ. Investigation of in vivo potential of scorpion venom against skin tumorigenesis in mice via targeting markers associated with cancer development. Drug Des Devel Ther. 2016;10:3387–3397. doi:10.2147/DDDT.S113171
  • LiuX, ChangY, ReinhartPH, SontheimerH, ChangY. Cloning and characterization of glioma BK, a novel BK channel isoform highly expressed in human glioma cells. J Neurosci. 2002;22:1840–1849. doi:10.1523/JNEUROSCI.22-05-01840.200211880513
  • BlochM, OusingsawatJ, SimonR, et al. KCNMA1 gene amplification promotes tumor cell proliferation in human prostate cancer. Oncogene. 2007;26:2525–2534. doi:10.1038/sj.onc.121003617146446
  • OeggerliM, TianY, RuizC, et al. Role of KCNMA1 in breast cancer. PLoS One. 2012;7:e41664. doi:10.1371/journal.pone.004166422899999
  • RamírezA, VeraE, Gamboa-DomínguezA, LambertP, GariglioP, CamachoJ. Calcium-activated potassium channels as potential early markers of human cervical cancer. Oncol Lett. 2018;15(5):7249–7254. doi:10.3892/ol.2018.818729725443
  • HanX, WangF, YaoW, et al. Heat shock proteins and p53 play a critical role in K+ channel-mediated tumor cell proliferation and apoptosis. Apoptosis. 2007;12(10):1837–1846. doi:10.1007/s10495-007-0101-917624594
  • SongX, ZhangG, SunA, et al. Scorpion venom component III inhibits cell proliferation by modulating NF-kappaB activation in human leukemia cells. Exp Ther Med. 2012;4(1):146–150. doi:10.3892/etm.2012.54823060939
  • ShaoJ, KangN, LiuY, SongS, WuC, ZhangJ. Purification and characterization of an analgesic peptide from Buthus martensii Karsch. Biomed Chromatogr. 2007;21:1266–1271. doi:10.1002/(ISSN)1099-080117604360
  • MaR, CuiY, ZhouY, et al. Location of the analgesic domain of scorpion toxin BmK AGAP by mutagenesis of disulfide bridges. Biochem Biophys Res Commun. 2010;394:330–334. doi:10.1016/j.bbrc.2010.02.17920206129
  • KampoS, AhmmedB, ZhouT, et al. Scorpion venom analgesic peptide, BmK AGAP inhibits stemness, and epithelial-mesenchymal transition by down-regulating PTX3 in breast cancer. Front Oncol. 2019;9:21. doi:10.3389/fonc.2019.0002130740360
  • BrackenburyWJ. Voltage-gated sodium channels and metastatic disease. Channels. 2012;6:352–361. doi:10.4161/chan.2191022992466
  • UllrichN, SontheimerH. Biophysical and pharmacological characterization of chloride currents in human astrocytoma cells. Am J Physiol. 1996;270:C1511–C1521. doi:10.1152/ajpcell.1996.270.5.C15118967454
  • SoroceanuL, GillespieY, KhazaeliMB, SontheimerH. Use of chlorotoxin for targeting of primary brain tumors. Cancer Res. 1998;58:4871–4879.9809993
  • SoroceanuL, ManningTJ Jr, SontheimerH. Modulation of glioma cell migration and invasion using Cl(-) and K(+) ion channel blockers. J Neurosci. 1999;19:5942–5954. doi:10.1523/JNEUROSCI.19-14-05942.199910407033
  • LyonsSA, O’NealJ, SontheimerH. Chlorotoxin, a scorpion derived peptide, specifically binds to gliomas and tumors of neuroectodermal origin. Glia. 2002;39:162–173. doi:10.1002/(ISSN)1098-113612112367
  • DeshaneJ, GarnerCC, SontheimerH. Chlorotoxin inhibits glioma cell invasion via matrix metalloproteinase-2. J Biol Chem. 2003;278(6):4135–4144. doi:10.1074/jbc.M20566220012454020
  • JacobyDB, DyskinE, YalcinM, et al. Potent pleiotropic anti-angiogenic effects of TM601, a synthetic chlorotoxin peptide. Anticancer Res. 2010;30(1):39–46.20150615
  • SawayaRE, YamamotoM, GokaslanZL, et al. Expression and localization of 72 kDa type IV collagenase (MMP-2) in human malignant gliomas in vivo. Clin Exp Metastasis. 1996;14:35–42. doi:10.1007/BF001576848521615
  • DardevetL, RaniD, AzizTA, et al. Chlorotoxin: a helpful natural scorpion peptide to diagnose glioma and fight tumor invasion. Toxins (Basel). 2015;7(4):1079–1101. doi:10.3390/toxins704107925826056
  • MamelakAN, RosenfeldS, BucholzR, et al. Phase I single-dose study of intracavitary-administered iodine-131-TM-601 in adults with recurrent high-grade glioma. J Clin Oncol. 2006;24(22):3644–3650. doi:10.1200/JCO.2005.05.456916877732
  • WuX S1, JianXC, YinB, HeZJ. Development of the research on the application of chlorotoxin in imaging diagnostics and targeted therapies for tumors. Chin J Cancer. 2010;29(6):626–630. doi:10.5732/cjc.009.1035920507737
  • FuYJ, YinLT, LiangAH, et al. Therapeutic potential of chlorotoxin like neurotoxin from the Chinese scorpion for human gliomas. Neurosci Lett. 2007;412:62–67. doi:10.1016/j.neulet.2006.10.05617166663
  • FuYJ, AnN, ChanKG, et al. A model of BmK CT in inhibiting glioma cell migration via matrix metalloproteinase 2 from experimental and molecular dynamics simulation study. Biotechnol Lett. 2011;33:1309–1317. doi:10.1007/s10529-011-0587-721424168
  • JangSH, ChoISY, RyuPD, LeeSY. Anti-proliferative effect of Kv1.3 blockers in A549 human lung adenocarcinoma in vitro and in vivo. Eur J Pharmacol. 2011;651:26–32. doi:10.1016/j.ejphar.2010.10.06621087602
  • FeskeS, WulffH, SkolnikEY. Ion channels in innate and adaptive immunity. Annu Rev Immunol. 2015;33:291–353. doi:10.1146/annurev-immunol-032414-11221225861976
  • MikaelianA. Polarized scorpion venom solution and method for making polarized venom solution. US 2009/0123558 A1 and US8097284B2. 2009 14 May and 2012 17 Jan.
  • FrankfurtOS, KrishanA. Apoptosis-based drug screening and detection of selective toxicity to cancer cells. Anticancer Drugs. 2003;14(7):555–561. doi:10.1097/00001813-200308000-0000812960740
  • DeBinJA, MaggioJE, StrichartzGR. Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion. Am J Physiol. 1993;264:361–369. doi:10.1152/ajpcell.1993.264.2.C361
  • GoudetC, ChiCW, TytgatJ. An overview of toxins and genes from the venom of the Asian scorpion Buthus martensi Karsch. Toxicon. 2002;40:1239–1258. doi:10.1016/S0041-0101(02)00142-312220709
  • AliSA, AlamM, AbbasiA, et al. Structure-activity relationship of chlorotoxin-like peptides. Toxins (Basel). 2016;8(2):36. doi:10.3390/toxins802003626848686
  • PossaniLD, MerinoE, CoronaM, BolivarF, BecerrilB. Peptides and genes coding for scorpion toxins that affect ion-channels. Biochimie. 2000;82:861–868. doi:10.1016/S0300-9084(00)01167-611086216
  • ValdiviaHH, KirbyMS, LedererWJ, CoronadoR. Scorpion toxins targeted against the sarcoplasmic reticulum Ca+2-release channel of skeletal and cardiac muscle. Proc Natl Acad Sci USA. 1992;89:12185–12189. doi:10.1073/pnas.89.24.121851334561
  • PossaniLD, BecerrilB, DelepierreM, TytgatJ. Scorpion toxins specific for Na+-channels. Eur J Biochem. 1999;264:287–300. doi:10.1046/j.1432-1327.1999.00625.x10491073
  • DuQ, HouX, GeL, et al. Cationicity-enhanced analogues of the antimicrobial peptides, AcrAP1 and AcrAP2, from the venom of the scorpion, Androctonus crassicauda, display potent growth modulation effects on human cancer cell lines. Int J Biol Sci. 2014;10:1097–1107. doi:10.7150/ijbs.985925332684
  • GuoX, MaC, DuQ, et al. Two peptides, TsAP-1 and TsAP-2, from the venom of the Brazilian yellow scorpion, Tityus serrulatus: evaluation of their antimicrobial and anticancer activities. Biochimie. 2013;95(9):1784. doi:10.1016/j.biochi.2013.06.00323770440
  • PedronCN, de OliveiraCS, da SilvaAF, et al. The effect of lysine substitutions in the biological activities of the scorpion venom peptide VmCT1. Eur J Pharm Sci. 2019;136:104952. doi:10.1016/j.ejps.2019.06.00631181304
  • Parrish-NovakJ, Byrnes-BlakeK, LalayevaN, et al. Nonclinical profile of BLZ-100, a tumor-targeting fluorescent imaging agent. Int J Toxicol. 2017;36(2):104–112. doi:10.1177/109158181769768528403743
  • PatilCG, WalkerDG, MillerDM, et al. Phase 1 safety, pharmacokinetics, and fluorescence imaging study of Tozuleristide (BLZ-100) in adults with newly diagnosed or recurrent gliomas. Neurosurgery. 2019:nyz125. doi:10.1093/neuros/nyz125