Covid-19 Research

Review Article

OCLC Number/Unique Identifier: 9385828661

Therapeutic Application of Genetically Engineered Ribosome-Inactivating Toxin Proteins for Cancer

Medicine Group    Start Submission

Safir Ullah Khan* and Munir Ullah Khan

Volume2-Issue12
Dates: Received: 2021-12-10 | Accepted: 2021-12-21 | Published: 2021-12-22
Pages: 1216-1228

Abstract

Recently, Ribosome-Inactivating Proteins (RIPs) as a class of anticancer medicines have garnered considerable attention due to their novel anticancer mechanism. Although the medications are small, RIPs utilize the Large-Size Effect (LSE) to block the efflux procedure that are regulated through Drug Resistance Transporters (DRTs), and protect host cells from drug transfection. There are many significant challenges for their therapeutic applications that seriously restrict their usefulness, particularly their strategy towards tumor cells. The primary objective of this review is to emphasize Trichosanthin (TCS) along with Gelonin (Gel) and additional types of RIPs, particularly scorpion venom-derived RIPs, to demonstrate that they should be grappling through what kinds of bio-barriers to overcome in cancer therapeutic science. Next, we will emphasize the latest state-of-the-art in providing cancer treatment RIPs.

FullText HTML FullText PDF DOI: 10.37871/jbres1375


Certificate of Publication




Copyright

© 2021 Khan SU, et al. Distributed under Creative Commons CC-BY 4.0

How to cite this article

Khan SU, Khan MU. Therapeutic Application of Genetically Engineered Ribosome-Inactivating Toxin Proteins for Cancer. J Biomed Res Environ Sci. 2021 Dec 22; 2(12): 1216-1228. doi: 10.37871/jbres1375, Article ID: JBRES1375, Available at: https://www.jelsciences.com/articles/jbres1375.pdf


Subject area(s)

References


  1. Shapira A, Benhar I. Toxin-based therapeutic approaches. Toxins. 2010;2(11):2519-2583. doi: 10.3390/toxins2112519.
  2. Maraganore JM, Joseph M, Bailey MC. Purification and characterization of trichosanthin. Homology to the ricin A chain and implications as to mechanism of abortifacient activity. J Biol Chem. 1987 Aug 25;262(24):11628-33. PMID: 3624228.
  3. Shi WW, Wong KB, Shaw PC. Structural and Functional Investigation and Pharmacological Mechanism of Trichosanthin, a Type 1 Ribosome-Inactivating Protein. Toxins (Basel). 2018 Aug 20;10(8):335. doi: 10.3390/toxins10080335. PMID: 30127254; PMCID: PMC6115768.
  4. Zhang C, Gong Y, Ma H, An C, Chen D, Chen ZL. Reactive oxygen species involved in trichosanthin-induced apoptosis of human choriocarcinoma cells. Biochem J. 2001 May 1;355(Pt 3):653-61. doi: 10.1042/bj3550653. Erratum in: Biochem J 2001 Sep 15;358(Pt 3):792. PMID: 11311127; PMCID: PMC1221780.
  5. Li M, Li X, Li JC. Possible mechanisms of trichosanthin-induced apoptosis of tumor cells. Anat Rec (Hoboken). 2010 Jun;293(6):986-92. doi: 10.1002/ar.21142. PMID: 20225201.
  6. Sha O, Niu J, Ng TB, Cho EY, Fu X, Jiang W. Anti-tumor action of trichosanthin, a type 1 ribosome-inactivating protein, employed in traditional Chinese medicine: a mini review. Cancer Chemother Pharmacol. 2013 Jun;71(6):1387-93. doi: 10.1007/s00280-013-2096-y. Epub 2013 Feb 3. PMID: 23377374; PMCID: PMC3668121.
  7. Fang EF, Ng TB, Shaw PC, Wong RN. Recent progress in medicinal investigations on trichosanthin and other ribosome inactivating proteins from the plant genus Trichosanthes. Curr Med Chem. 2011;18(28):4410-7. doi: 10.2174/092986711797200499. PMID: 21861819.
  8. Li Z, Qu Y, Li H, Yuan J. Truncations of gelonin lead to a reduction in its cytotoxicity. Toxicology. 2007 Mar 7;231(2-3):129-36. doi: 10.1016/j.tox.2006.11.074. Epub 2006 Dec 8. PMID: 17222956.
  9. Wang P, Chen LL, Yan H, Li JC. Trichosanthin suppresses HeLa cell proliferation through inhibition of the PKC/MAPK signaling pathway. Cell Biol Toxicol. 2009 Oct;25(5):479-88. doi: 10.1007/s10565-008-9102-x. Epub 2008 Aug 28. PMID: 18751959.
  10. Jiang Q, Bai T, Shen S, Li L, Ding H, Wang P. Increase of cytosolic calcium induced by trichosanthin suppresses cAMP/PKC levels through the inhibition of adenylyl cyclase activity in HeLa cells. Mol Biol Rep. 2011 Apr;38(4):2863-8. doi: 10.1007/s11033-010-0432-4. Epub 2010 Nov 19. PMID: 21088904.
  11. Kang M, Ou H, Wang R, Liu W, Mao Y, Tang A. Effect of trichosanthin on apoptosis and telomerase activity of nasopharyngeal carcinomas in nude mice. J BUON. 2013 Jul-Sep;18(3):675-82. PMID: 24065482.
  12. Huang Y, Song H, Hu H, Cui L, You C, Huang L. Trichosanthin inhibits DNA methyltransferase and restores methylation-silenced gene expression in human cervical cancer cells. Mol Med Rep. 2012 Oct;6(4):872-8. doi: 10.3892/mmr.2012.994. Epub 2012 Jul 18. PMID: 22825485.
  13. Cui L, Song J, Wu L, Huang L, Wang Y, Huang Y, Yu H, Huang Y, You CC, Ye J. Smac is another pathway in the anti-tumour activity of Trichosanthin and reverses Trichosanthin resistance in CaSki cervical cancer cells. Biomed Pharmacother. 2015 Feb;69:119-24. doi: 10.1016/j.biopha.2014.10.027. Epub 2014 Nov 11. PMID: 25661347.
  14. Chen GF, Huang WG, Chen FY, Shan JL. [Protective effects of trichosanthin in Herpes simplex virus-1 encephalitis in mice]. Zhongguo Dang Dai Er Ke Za Zhi. 2006 Jun;8(3):239-41. Chinese. PMID: 16787600.
  15. Fang EF, Zhang CZ, Zhang L, Wong JH, Chan YS, Pan WL, Dan XL, Yin CM, Cho CH, Ng TB. Trichosanthin inhibits breast cancer cell proliferation in both cell lines and nude mice by promotion of apoptosis. PLoS One. 2012;7(9):e41592. doi: 10.1371/journal.pone.0041592. Epub 2012 Sep 5. PMID: 22957017; PMCID: PMC3434199.
  16. Wang JH, Nie HL, Tam SC, Huang H, Zheng YT. Anti-HIV-1 property of trichosanthin correlates with its ribosome inactivating activity. FEBS Lett. 2002 Nov 6;531(2):295-8. doi: 10.1016/s0014-5793(02)03539-1. PMID: 12417329.
  17. Stirpe F, Olsnes S, Pihl A. Gelonin, a new inhibitor of protein synthesis, nontoxic to intact cells. Isolation, characterization, and preparation of cytotoxic complexes with concanavalin A. J Biol Chem. 1980 Jul 25;255(14):6947-53. PMID: 7391060.
  18. Pagliaro LC, Liu B, Munker R, Andreeff M, Freireich EJ, Scheinberg DA, Rosenblum MG. Humanized M195 monoclonal antibody conjugated to recombinant gelonin: an anti-CD33 immunotoxin with antileukemic activity. Clin Cancer Res. 1998 Aug;4(8):1971-6. PMID: 9717827.
  19. Varkouhi AK, Scholte M, Storm G, Haisma HJ. Endosomal escape pathways for delivery of biologicals. J Control Release. 2011 May 10;151(3):220-8. doi: 10.1016/j.jconrel.2010.11.004. Epub 2010 Nov 13. PMID: 21078351.
  20. Nicolas E, Beggs JM, Haltiwanger BM, Taraschi TF. Direct evidence for the deoxyribonuclease activity of the plant ribosome inactivating protein gelonin. FEBS Lett. 1997 Apr 7;406(1-2):162-4. doi: 10.1016/s0014-5793(97)00267-6. PMID: 9109409.
  21. Shin MC, Zhang J, David AE, Trommer WE, Kwon YM, Min KA, Kim JH, Yang VC. Chemically and biologically synthesized CPP-modified gelonin for enhanced anti-tumor activity. J Control Release. 2013 Nov 28;172(1):169-178. doi: 10.1016/j.jconrel.2013.08.016. Epub 2013 Aug 23. PMID: 23973813; PMCID: PMC3849409.
  22. Nolan PA, Garrison DA, Better M. Cloning and expression of a gene encoding gelonin, a ribosome-inactivating protein from Gelonium multiflorum. Gene. 1993 Dec 8;134(2):223-7. doi: 10.1016/0378-1119(93)90097-m. PMID: 7916721.
  23. Park T, Min KA, Cheong H, Moon C, Shin MC. Genetic engineering and characterisation of chlorotoxin-fused gelonin for enhanced glioblastoma therapy. J Drug Target. 2019 Nov;27(9):950-958. doi: 10.1080/1061186X.2018.1516221. Epub 2018 Sep 11. PMID: 30156929.
  24. Veenendaal LM, Jin H, Ran S, Cheung L, Navone N, Marks JW, Waltenberger J, Thorpe P, Rosenblum MG. In vitro and in vivo studies of a VEGF121/rGelonin chimeric fusion toxin targeting the neovasculature of solid tumors. Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):7866-71. doi: 10.1073/pnas.122157899. Erratum in: Proc Natl Acad Sci U S A 2002 Aug 6;99(16):10941. PMID: 12060733; PMCID: PMC122986.
  25. Lyu MA, Cheung LH, Hittelman WN, Marks JW, Aguiar RC, Rosenblum MG. The rGel/BLyS fusion toxin specifically targets malignant B cells expressing the BLyS receptors BAFF-R, TACI, and BCMA. Mol Cancer Ther. 2007 Feb;6(2):460-70. doi: 10.1158/1535-7163.MCT-06-0254. Epub 2007 Jan 31. PMID: 17267661.
  26. Lyu MA, Rai D, Ahn KS, Sung B, Cheung LH, Marks JW, Aggarwal BB, Aguiar RC, Gandhi V, Rosenblum MG. The rGel/BLyS fusion toxin inhibits diffuse large B-cell lymphoma growth in vitro and in vivo. Neoplasia. 2010 May;12(5):366-75. doi: 10.1593/neo.91960. PMID: 20454508; PMCID: PMC2864474.
  27. Nimmanapalli R, Lyu MA, Du M, Keating MJ, Rosenblum MG, Gandhi V. The growth factor fusion construct containing B-lymphocyte stimulator (BLyS) and the toxin rGel induces apoptosis specifically in BAFF-R-positive CLL cells. Blood. 2007 Mar 15;109(6):2557-64. doi: 10.1182/blood-2006-08-042424. Epub 2006 Nov 21. PMID: 17119117.
  28. Lyu MA, Cao YJ, Mohamedali KA, Rosenblum MG. Cell-targeting fusion constructs containing recombinant gelonin. Methods Enzymol. 2012;502:167-214. doi: 10.1016/B978-0-12-416039-2.00008-2. PMID: 22208986.
  29. Ham S, Min KA, Yang JW, Shin MC. Fusion of gelonin and anti-insulin-like growth factor-1 receptor (IGF-1R) affibody for enhanced brain cancer therapy. Arch Pharm Res. 2017 Sep;40(9):1094-1104. doi: 10.1007/s12272-017-0953-7. Epub 2017 Sep 12. PMID: 28900896.
  30. Shin MC, Min KA, Cheong H, Moon C, Huang Y, He H, Yang VC. Preparation and Characterization of Gelonin-Melittin Fusion Biotoxin for Synergistically Enhanced Anti-Tumor Activity. Pharm Res. 2016 Sep;33(9):2218-2228. doi: 10.1007/s11095-016-1959-4. Epub 2016 Jun 1. PMID: 27251414; PMCID: PMC4967393.
  31. Ham SH, Min KA, Shin MC. Molecular tumor targeting of gelonin by fusion with F3 peptide. Acta Pharmacol Sin. 2017 Jun;38(6):897-906. doi: 10.1038/aps.2017.20. Epub 2017 Apr 17. PMID: 28414205; PMCID: PMC5520187.
  32. Esser C, Rannug A. The aryl hydrocarbon receptor in barrier organ physiology, immunology, and toxicology. Pharmacol Rev. 2015;67(2):259-79. doi: 10.1124/pr.114.009001. PMID: 25657351.
  33. Pohorille A, Deamer D. Self-assembly and function of primitive cell membranes. Res Microbiol. 2009 Sep;160(7):449-56. doi: 10.1016/j.resmic.2009.06.004. Epub 2009 Jul 4. PMID: 19580865.
  34. Chenab KK, Eivazzadeh-Keihan R, Maleki A, Pashazadeh-Panahi P, Hamblin MR, Mokhtarzadeh A. Biomedical applications of nanoflares: Targeted intracellular fluorescence probes. Nanomedicine. 2019 Apr;17:342-358. doi: 10.1016/j.nano.2019.02.006. Epub 2019 Feb 28. PMID: 30826476; PMCID: PMC6520197.
  35. Su C, Liu Y, Li R, Wu W, Fawcett JP, Gu J. Absorption, distribution, metabolism and excretion of the biomaterials used in Nanocarrier drug delivery systems. Adv Drug Deliv Rev. 2019 Mar 15;143:97-114. doi: 10.1016/j.addr.2019.06.008. Epub 2019 Jun 28. PMID: 31255595.
  36. Jones AR, Shusta EV. Blood-brain barrier transport of therapeutics via receptor-mediation. Pharm Res. 2007 Sep;24(9):1759-71. doi: 10.1007/s11095-007-9379-0. Epub 2007 Jul 10. PMID: 17619996; PMCID: PMC2685177.
  37. Upadhyay RK. Drug delivery systems, CNS protection, and the blood brain barrier. Biomed Res Int. 2014;2014:869269. doi: 10.1155/2014/869269. Epub 2014 Jul 20. PMID: 25136634; PMCID: PMC4127280.
  38. High KP. Overcoming barriers to adult immunization. J Am Osteopath Assoc. 2009 Jun;109(6 Suppl 2):S25-8. PMID: 19553634.
  39. Xu W, Hou W, Yao G, Ji Y, Yeh M, Sun B. Inhibition of Th1- and enhancement of Th2-initiating cytokines and chemokines in trichosanthin- treated macrophages. Biochem Biophys Res Commun. 2001 Jun 1;284(1):168-72. doi: 10.1006/bbrc.2001.4940. PMID: 11374886.
  40. Madan S, Ghosh PC. Interaction of gelonin with macrophages: effect of lysosomotropic amines. Exp Cell Res. 1992 Jan;198(1):52-8. doi: 10.1016/0014-4827(92)90148-2. PMID: 1727057.
  41. Zervantonakis IK, Hughes-Alford SK, Charest JL, Condeelis JS, Gertler FB, Kamm RD. Three-dimensional microfluidic model for tumor cell intravasation and endothelial barrier function. Proc Natl Acad Sci U S A. 2012 Aug 21;109(34):13515-20. doi: 10.1073/pnas.1210182109. Epub 2012 Aug 6. PMID: 22869695; PMCID: PMC3427099.
  42. Azzi S, Hebda JK, Gavard J. Vascular permeability and drug delivery in cancers. Front Oncol. 2013 Aug 15;3:211. doi: 10.3389/fonc.2013.00211. PMID: 23967403; PMCID: PMC3744053.
  43. Simonsen TG, Gaustad JV, Leinaas MN, Rofstad EK. High interstitial fluid pressure is associated with tumor-line specific vascular abnormalities in human melanoma xenografts. PLoS One. 2012;7(6):e40006. doi: 10.1371/journal.pone.0040006. Epub 2012 Jun 29. PMID: 22768196; PMCID: PMC3386940.
  44. Walker C, Mojares E, Del Río Hernández A. Role of Extracellular Matrix in Development and Cancer Progression. Int J Mol Sci. 2018 Oct 4;19(10):3028. doi: 10.3390/ijms19103028. PMID: 30287763; PMCID: PMC6213383.
  45. Eble JA, Niland S. The extracellular matrix in tumor progression and metastasis. Clin Exp Metastasis. 2019 Jun;36(3):171-198. doi: 10.1007/s10585-019-09966-1. Epub 2019 Apr 11. PMID: 30972526.
  46. Au JL, Yeung BZ, Wientjes MG, Lu Z, Wientjes MG. Delivery of cancer therapeutics to extracellular and intracellular targets: Determinants, barriers, challenges and opportunities. Adv Drug Deliv Rev. 2016 Feb 1;97:280-301. doi: 10.1016/j.addr.2015.12.002. Epub 2015 Dec 11. PMID: 26686425; PMCID: PMC4829347.
  47. Chen B, Le W, Wang Y, Li Z, Wang D, Ren L, Lin L, Cui S, Hu JJ, Hu Y, Yang P, Ewing RC, Shi D, Cui Z. Targeting Negative Surface Charges of Cancer Cells by Multifunctional Nanoprobes. Theranostics. 2016 Aug 7;6(11):1887-98. doi: 10.7150/thno.16358. PMID: 27570558; PMCID: PMC4997244.
  48. Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol. 2009 Sep;10(9):597-608. doi: 10.1038/nrm2755. PMID: 19696797; PMCID: PMC3038567.
  49. Shin MC, Zhang J, Min KA, Lee K, Byun Y, David AE, He H, Yang VC. Cell-penetrating peptides: achievements and challenges in application for cancer treatment. J Biomed Mater Res A. 2014 Feb;102(2):575-87. doi: 10.1002/jbm.a.34859. Epub 2013 Jul 30. PMID: 23852939; PMCID: PMC3929953.
  50. Chen Y, Zhang M, Min KA, Wang H, Shin MC, Li F, Yang VC, Huang Y. Improved Protein Toxin Delivery Based on ATTEMPTS Systems. Curr Drug Targets. 2018 Feb 19;19(4):380-392. doi: 10.2174/1389450118666170302094758. PMID: 28260497; PMCID: PMC5581292.
  51. Powell AK, Yates EA, Fernig DG, Turnbull JE. Interactions of heparin/heparan sulfate with proteins: appraisal of structural factors and experimental approaches. Glycobiology. 2004 Apr;14(4):17R-30R. doi: 10.1093/glycob/cwh051. Epub 2004 Jan 12. PMID: 14718374.
  52. Wang H, Moon C, Shin MC, Wang Y, He H, Yang VC, Huang Y. Heparin-Regulated Prodrug-Type Macromolecular Theranostic Systems for Cancer Therapy. Nanotheranostics. 2017 Mar 3;1(1):114-130. doi: 10.7150/ntno.18292. PMID: 29071181; PMCID: PMC5646728.
  53. Shin MC, Zhang J, Min KA, He H, David AE, Huang Y, Yang VC. PTD-Modified ATTEMPTS for Enhanced Toxin-based Cancer Therapy: An In Vivo Proof-of-Concept Study. Pharm Res. 2015 Aug;32(8):2690-703. doi: 10.1007/s11095-015-1653-y. Epub 2015 Feb 21. PMID: 25701313; PMCID: PMC4490053.
  54. Shin MC, Zhao J, Zhang J, Huang Y, He H, Wang M, Min KA, Yang VC. Recombinant TAT-gelonin fusion toxin: synthesis and characterization of heparin/protamine-regulated cell transduction. J Biomed Mater Res A. 2015 Jan;103(1):409-419. doi: 10.1002/jbm.a.35188. Epub 2014 Apr 23. PMID: 24733757; PMCID: PMC4198515.
  55. Shin MC, Zhao J, Zhang J, Huang Y, He H, Wang M, Min KA, Yang VC. Recombinant TAT-gelonin fusion toxin: synthesis and characterization of heparin/protamine-regulated cell transduction. J Biomed Mater Res A. 2015 Jan;103(1):409-419. doi: 10.1002/jbm.a.35188. Epub 2014 Apr 23. PMID: 24733757; PMCID: PMC4198515.
  56. Chen Y, Zhang M, Jin H, Li D, Xu F, Wu A, Wang J, Huang Y. Glioma Dual-Targeting Nanohybrid Protein Toxin Constructed by Intein-Mediated Site-Specific Ligation for Multistage Booster Delivery. Theranostics. 2017 Aug 15;7(14):3489-3503. doi: 10.7150/thno.20578. PMID: 28912890; PMCID: PMC5596438.
  57. Chen Y, Zhang M, Jin H, Tang Y, Wang H, Xu Q, Li Y, Li F, Huang Y. Intein-mediated site-specific synthesis of tumor-targeting protein delivery system: Turning PEG dilemma into prodrug-like feature. Biomaterials. 2017 Feb;116:57-68. doi: 10.1016/j.biomaterials.2016.11.033. Epub 2016 Nov 27. PMID: 27914267; PMCID: PMC5527826.
  58. Chen Y, Zhang M, Jin H, Tang Y, Wu A, Xu Q, Huang Y. Prodrug-Like, PEGylated Protein Toxin Trichosanthin for Reversal of Chemoresistance. Mol Pharm. 2017 May 1;14(5):1429-1438. doi: 10.1021/acs.molpharmaceut.6b00987. Epub 2017 Feb 14. PMID: 28195491.
  59. Kato Y, Ozawa S, Miyamoto C, Maehata Y, Suzuki A, Maeda T, Baba Y. Acidic extracellular microenvironment and cancer. Cancer Cell Int. 2013 Sep 3;13(1):89. doi: 10.1186/1475-2867-13-89. PMID: 24004445; PMCID: PMC3849184.
  60. Reshetnyak YK. Imaging Tumor Acidity: pH-Low Insertion Peptide Probe for Optoacoustic Tomography. Clin Cancer Res. 2015 Oct 15;21(20):4502-4. doi: 10.1158/1078-0432.CCR-15-1502. Epub 2015 Jul 29. PMID: 26224874; PMCID: PMC4609264.
  61. Khanmohammadi Chenab K, Sohrabi B, Esrafli M. pHsensitive organic diimide materials-based superhydrophobic surface for oil-water separation applications. Mater Res Express. 2020; 6(12):125112.
  62. Vila-Caballer M, Codolo G, Munari F, Malfanti A, Fassan M, Rugge M, Balasso A, de Bernard M, Salmaso S. A pH-sensitive stearoyl-PEG-poly(methacryloyl sulfadimethoxine)-decorated liposome system for protein delivery: An application for bladder cancer treatment. J Control Release. 2016 Sep 28;238:31-42. doi: 10.1016/j.jconrel.2016.07.024. Epub 2016 Jul 18. PMID: 27444816.
  63. Kisovec M, Rezelj S, Knap P, Cajnko MM, Caserman S, Flašker A, Žnidaršič N, Repič M, Mavri J, Ruan Y, Scheuring S, Podobnik M, Anderluh G. Engineering a pH responsive pore forming protein. Sci Rep. 2017 Feb 8;7:42231. doi: 10.1038/srep42231. PMID: 28176876; PMCID: PMC5296754.
  64. Khanmohammadi Chenab K, Sohrabi B, Jafari A, Ramakrishna S. Water treatment: functional nanomaterials and applications from adsorption to photodegradation. Mater Today Chem 2020;16:100262. doi: 10.1016/j.mtchem. 2020.100262.
  65. Khanmohammadi Chenab K, Sohrabi B, Jafari A, Ramakrishna S. Effect of electron-donating and -withdrawing substitutions in naphthoquinone sensitizers: the structure engineering of dyes for DSSCs. J Mol Struct. 2018;1167:274–279. doi: 10.1016/j.molstruc.2018.05.014.
  66. Khanmohammadi Chenab K, Sohrabi B, Zamani Meymian MR, Mousavi SV. Naphthoquinone derivative-based dye for dye-sensitized solar cells: experimental and computational aspects. Mater Res Express 2019;6(8):085537.
  67. Khanmohammadi Chenab K, Sohrabi B, Zamani Meymian MR.
  68. Cobalt complex dye as a novel sensitizer in dye sensitized solar cells. Mater Res Express. 2020;6(12):125536.
  69. Khanmohammadi Chenab K. Anti-Icing Properties of vertically aligned TiO2 nanopillars. Langmuir. 2020; 36(21):6041–6050. doi: /10.1021/acs.langmuir.0c00093.
  70. Eivazzadeh-Keihan R, Maleki A, de la Guardia M, Bani MS, Chenab KK, Pashazadeh-Panahi P, Baradaran B, Mokhtarzadeh A, Hamblin MR. Carbon based nanomaterials for tissue engineering of bone: Building new bone on small black scaffolds: A review. J Adv Res. 2019 Mar 28;18:185-201. doi: 10.1016/j.jare.2019.03.011. PMID: 31032119; PMCID: PMC6479020.
  71. Eivazzadeh-Keihan R, Chenab KK, Taheri-Ledari R, Mosafer J, Hashemi SM, Mokhtarzadeh A, Maleki A, Hamblin MR. Recent advances in the application of mesoporous silica-based nanomaterials for bone tissue engineering. Mater Sci Eng C Mater Biol Appl. 2020 Feb;107:110267. doi: 10.1016/j.msec.2019.110267. Epub 2019 Oct 15. PMID: 31761248; PMCID: PMC6907012.
  72. Eivazzadeh-Keihan R, Bahojb Noruzi E, Khanmohammadi Chenab K, Jafari A, Radinekiyan F, Hashemi SM, Ahmadpour F, Behboudi A, Mosafer J, Mokhtarzadeh A, Maleki A, Hamblin MR. Metal-based nanoparticles for bone tissue engineering. J Tissue Eng Regen Med. 2020 Dec;14(12):1687-1714. doi: 10.1002/term.3131. Epub 2020 Sep 30. PMID: 32914573.
  73. Khanmohammadi Chenab K, Sohrabi B, Rahmanzadeh A. Superhydrophobicity: advanced biological and biomedical applications. Biomater Sci. 2019 Aug 1;7(8):3110-3137. doi: 10.1039/c9bm00558g. Epub 2019 Jun 19. PMID: 31215913.
  74. Zhang M, Liu E, Cui Y, Huang Y. Nanotechnology-based combination therapy for overcoming multidrug-resistant cancer. Cancer Biol Med. 2017 Aug;14(3):212-227. doi: 10.20892/j.issn.2095-3941.2017.0054. PMID: 28884039; PMCID: PMC5570599.
  75. Pizzo E, Di Maro A. A new age for biomedical applications of Ribosome Inactivating Proteins (RIPs): from bioconjugate to nanoconstructs. J Biomed Sci. 2016 Jul 20;23(1):54. doi: 10.1186/s12929-016-0272-1. PMID: 27439918; PMCID: PMC4955249.
  76. Provoda CJ, Stier EM, Lee KD. Tumor cell killing enabled by listeriolysin O-liposome-mediated delivery of the protein toxin gelonin. J Biol Chem. 2003 Sep 12;278(37):35102-8. doi: 10.1074/jbc.M305411200. Epub 2003 Jun 27. PMID: 12832408.
  77. Tang Y, Liang J, Wu A, Chen Y, Zhao P, Lin T, Zhang M, Xu Q, Wang J, Huang Y. Co-Delivery of Trichosanthin and Albendazole by Nano-Self-Assembly for Overcoming Tumor Multidrug-Resistance and Metastasis. ACS Appl Mater Interfaces. 2017 Aug 16;9(32):26648-26664. doi: 10.1021/acsami.7b05292. Epub 2017 Aug 3. Erratum in: ACS Appl Mater Interfaces. 2020 Jan 15;12(2):3275. PMID: 28741923.
  78. Martinez de Pinillos Bayona A, Moore CM, Loizidou M, MacRobert AJ, Woodhams JH. Enhancing the efficacy of cytotoxic agents for cancer therapy using photochemical internalisation. Int J Cancer. 2016 Mar 1;138(5):1049-57. doi: 10.1002/ijc.29510. Epub 2015 Mar 23. PMID: 25758607; PMCID: PMC4973841.
  79. Bull-Hansen B, Berstad MB, Berg K, Cao Y, Skarpen E, Fremstedal AS, Rosenblum MG, Peng Q, Weyergang A. Photochemical activation of MH3-B1/rGel: a HER2-targeted treatment approach for ovarian cancer. Oncotarget. 2015 May 20;6(14):12436-51. doi: 10.18632/oncotarget.3814. PMID: 26002552; PMCID: PMC4494949.
  80. Berstad MB, Cheung LH, Berg K, Peng Q, Fremstedal AS, Patzke S, Rosenblum MG, Weyergang A. Design of an EGFR-targeting toxin for photochemical delivery: in vitro and in vivo selectivity and efficacy. Oncogene. 2015 Oct 29;34(44):5582-92. doi: 10.1038/onc.2015.15. Epub 2015 Feb 16. PMID: 25684137.
  81. Dietze A, Peng Q, Selbo PK, Kaalhus O, Müller C, Bown S, Berg K. Enhanced photodynamic destruction of a transplantable fibrosarcoma using photochemical internalisation of gelonin. Br J Cancer. 2005 Jun 6;92(11):2004-9. doi: 10.1038/sj.bjc.6602600. PMID: 15886704; PMCID: PMC2361782.
  82. Berg K, Selbo PK, Prasmickaite L, Tjelle TE, Sandvig K, Moan J, Gaudernack G, Fodstad O, Kjølsrud S, Anholt H, Rodal GH, Rodal SK, Høgset A. Photochemical internalization: a novel technology for delivery of macromolecules into cytosol. Cancer Res. 1999 Mar 15;59(6):1180-3. PMID: 10096543.
  83. Weyergang A, Fremstedal AS, Skarpen E, Peng Q, Mohamedali KA, Eng MS, Cheung LH, Rosenblum MG, Waltenberger J, Berg K. Light-enhanced VEGF121/rGel: A tumor targeted modality with vascular and immune-mediated efficacy. J Control Release. 2018 Oct 28;288:161-172. doi: 10.1016/j.jconrel.2018.09.005. Epub 2018 Sep 11. PMID: 30217739.
  84. Catterall WA, Goldin AL, Waxman SG. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev. 2005 Dec;57(4):397-409. doi: 10.1124/pr.57.4.4. PMID: 16382098.
  85. Catterall WA. Structure and function of voltage-gated ion channels. Annu Rev Biochem. 1995;64:493-531. doi: 10.1146/annurev.bi.64.070195.002425. PMID: 7574491.
  86. Payandeh J, Scheuer T, Zheng N, Catterall WA. The crystal structure of a voltage-gated sodium channel. Nature. 2011 Jul 10;475(7356):353-8. doi: 10.1038/nature10238. PMID: 21743477; PMCID: PMC3266868.
  87. Zhang F, Xu X, Li T, Liu Z. Shellfish toxins targeting voltage-gated sodium channels. Mar Drugs. 2013 Nov 28;11(12):4698-723. doi: 10.3390/md11124698. PMID: 24287955; PMCID: PMC3877881.
  88. Cestèle S, Catterall WA. Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie. 2000 Sep-Oct;82(9-10):883-92. doi: 10.1016/s0300-9084(00)01174-3. PMID: 11086218.
  89. Lewis RJ, Garcia ML. Therapeutic potential of venom peptides. Nat Rev Drug Discov. 2003 Oct;2(10):790-802. doi: 10.1038/nrd1197. PMID: 14526382.
  90. Morales-Lázaro SL, Hernández-García E, Serrano-Flores B, Rosenbaum T. Organic toxins as tools to understand ion channel mechanisms and structure. Curr Top Med Chem. 2015;15(7):581-603. doi: 10.2174/1568026615666150217110710. PMID: 25686735.
  91. Girault A, Haelters JP, Potier-Cartereau M, Chantôme A, Jaffrés PA, Bougnoux P, Joulin V, Vandier C. Targeting SKCa channels in cancer: potential new therapeutic approaches. Curr Med Chem. 2012;19(5):697-713. doi: 10.2174/092986712798992039. PMID: 22204342.
  92. Potier M, Joulin V, Roger S, Besson P, Jourdan ML, Leguennec JY, Bougnoux P, Vandier C. Identification of SK3 channel as a new mediator of breast cancer cell migration. Mol Cancer Ther. 2006 Nov;5(11):2946-53. doi: 10.1158/1535-7163.MCT-06-0194. PMID: 17121942.
  93. Brown BM, Shim H, Christophersen P, Wulff H. Pharmacology of Small- and Intermediate-Conductance Calcium-Activated Potassium Channels. Annu Rev Pharmacol Toxicol. 2020 Jan 6;60:219-240. doi: 10.1146/annurev-pharmtox-010919-023420. Epub 2019 Jul 23. PMID: 31337271.
  94. Jaffrès PA, Gajate C, Bouchet AM, Couthon-Gourvès H, Chantôme A, Potier-Cartereau M, Besson P, Bougnoux P, Mollinedo F, Vandier C. Alkyl ether lipids, ion channels and lipid raft reorganization in cancer therapy. Pharmacol Ther. 2016 Sep;165:114-31. doi: 10.1016/j.pharmthera.2016.06.003. Epub 2016 Jun 8. PMID: 27288726.
  95. Pedarzani P, D'hoedt D, Doorty KB, Wadsworth JD, Joseph JS, Jeyaseelan K, Kini RM, Gadre SV, Sapatnekar SM, Stocker M, Strong PN. Tamapin, a venom peptide from the Indian red scorpion (Mesobuthus tamulus) that targets small conductance Ca2+-activated K+ channels and afterhyperpolarization currents in central neurons. J Biol Chem. 2002 Nov 29;277(48):46101-9. doi: 10.1074/jbc.M206465200. Epub 2002 Sep 17. PMID: 12239213.
  96. Mayorga-Flores M, Chantôme A, Melchor-Meneses CM, Domingo I, Titaux-Delgado GA, Galindo-Murillo R, Vandier C, Del Río-Portilla F. Novel Blocker of Onco SK3 Channels Derived from Scorpion Toxin Tamapin and Active against Migration of Cancer Cells. ACS Med Chem Lett. 2020 Jul 10;11(8):1627-1633. doi: 10.1021/acsmedchemlett.0c00300. PMID: 32832033; PMCID: PMC7429966.
  97. Li C, Liu M, Monbo J, Zou G, Li C, Yuan W, Zella D, Lu WY, Lu W. Turning a scorpion toxin into an antitumor miniprotein. J Am Chem Soc. 2008 Oct 15;130(41):13546-8. doi: 10.1021/ja8042036. Epub 2008 Sep 18. PMID: 18798622; PMCID: PMC3810402.
  98. Akcan M, Stroud MR, Hansen SJ, Clark RJ, Daly NL, Craik DJ, Olson JM. Chemical re-engineering of chlorotoxin improves bioconjugation properties for tumor imaging and targeted therapy. J Med Chem. 2011 Feb 10;54(3):782-7. doi: 10.1021/jm101018r. Epub 2011 Jan 6. Erratum in: J Med Chem. 2013 Dec 12;56(23):9807. PMID: 21210710; PMCID: PMC3086956.
  99. Yu K, Fu W, Liu H, Luo X, Chen KX, Ding J, Shen J, Jiang H. Computational simulations of interactions of scorpion toxins with the voltage-gated potassium ion channel. Biophys J. 2004 Jun;86(6):3542-55. doi: 10.1529/biophysj.103.039461. PMID: 15189853; PMCID: PMC1304258.


Comments


Swift, Reliable, and studious. We aim to cherish the world by publishing precise knowledge.

  • asd
  • Brown University Library
  • University of Glasgow Library
  • University of Pennsylvania, Penn Library
  • University of Amsterdam Library
  • The University of British Columbia Library
  • UC Berkeley’s Library
  • MIT Libraries
  • Kings College London University
  • University of Texas Libraries
  • UNSW Sidney Library
  • The University of Hong Kong Libraries
  • UC Santa Barbara Library
  • University of Toronto Libraries
  • University of Oxford Library
  • Australian National University
  • ScienceOpen
  • UIC Library
  • KAUST University Library
  • Cardiff University Library
  • Ball State University Library
  • Duke University Library
  • Rutgers University Library
  • Air University Library
  • UNT University of North Texas
  • Washington Research Library Consortium
  • Penn State University Library
  • Georgetown Library
  • Princeton University Library
  • Science Gate
  • Internet Archive
  • WashingTon State University Library
  • Dimensions
  • Zenodo
  • OpenAire
  • Index Copernicus International
  • icmje
  •  International Scientific Indexing (ISI)
  • Sherpa Romeo
  • ResearchGate
  • Universidad De Lima
  • WorldCat
  • JCU Discovery
  • McGill
  • National University of Singepore Libraries
  • SearchIT
  • Scilit
  • SemantiScholar
  • Base Search
  • VU
  • KB
  • Publons
  • oaji
  • Harvard University
  • sjsu-library
  • UWLSearch
  • Florida Institute of Technology
  • CrossRef
  • LUBsearch
  • Universitat de Paris
  • Technical University of Denmark
  • ResearchBIB
  • Google Scholar
  • Microsoft Academic Search