772
Views
23
CrossRef citations to date
0
Altmetric
Review

Peptides as a therapeutic avenue for nanocarrier-aided targeting of glioma

&
Pages 811-824 | Received 18 Mar 2016, Accepted 26 Sep 2016, Published online: 11 Oct 2016

References

  • DeAngelis LM. Brain tumors. N Engl J Med. 2001;344:114–123.
  • Cojoc M, Mäbert K, Muders MH, et al. A role for cancer stem cells in therapy resistance: cellular and molecular mechanisms. Semin Cancer Biol. 2015;31:16–27.
  • Beier D, Schulz JB, Beier CP. Chemoresistance of glioblastoma cancer stem cells – much more complex than expected. Mol Cancer. 2011;10:128.
  • Achuthan S, Santhoshkumar TR, Prabhakar J, et al. Drug-induced senescence generates chemoresistant stemlike cells with low reactive oxygen species. J Biol Chem. 2011;286:37813–37829.
  • Sten Friberg S, Nyström AM. Nanomedicine: will it offer possibilities to overcome multiple drug resistance in cancer? J Nanobiotechnol. 2016;14:17.
  • Schwartzbaum JA, Fisher JL, Aldape KD, et al. Epidemiology and molecular pathology of glioma. Nat Clin Pract Neuro. 2006;2:494–503.
  • Grobben B, De Deyn PP, Slegers H. Rat C6 glioma as experimental model system for the study of glioblastoma growth and invasion. Cell Tissue Res. 2002;310:257–270.
  • Liu Y, Weiyue L. Recent advances in brain tumor-targeted nano-drug delivery systems. Expert Opin on Drug Deliv. 2012;9(6):671–686.
  • Bodor N, Buchwald P. Recent advances in the brain targeting of neuropharmaceuticals by chemical delivery systems. Adv Drug Deliv Rev. 1999;36:229–254.
  • Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis. 2004;16:1–13.
  • Chen Y, Liu L. Modern methods for delivery of drugs across the blood–brain barrier. Adv Drug Deliv Rev. 2012;64(7):640–665.
  • Pardridge WM. The blood-brain barrier: bottleneck in brain drug development. NeuroRx. 2005;2:3–14.
  • Pajouhesh H, Lenz GR. Medicinal chemical properties of successful central nervous system drugs. NeuroRx. 2005;2(4):541–553.
  • Zhu Y, Parada LF. The molecular and genetic basis of neurological tumours. Nat Rev Cancer. 2002;2:616–626.
  • Ohgaki H, Dessen P, Jourde B, et al. Genetic pathways to glioblastoma: a population-based study. Cancer Res. 2004;64:6892–6899.
  • Mrugala MM. Advances and challenges in the treatment of glioblastoma: a clinician’s perspective. Discov Med. 2013;15:221–230.
  • Li J, Di C, Mattox AK, et al. The future role of personalized medicine in the treatment of glioblastoma multiforme. Pharmgenomics Pers Med. 2010;3:111–127.
  • Patel MA, Kim JE, Ruzevick J, et al. The future of glioblastoma therapy: synergism of standard of care and immunotherapy. Cancers. 2014;6:1953–1985.
  • Jhanwar-Uniyal M, Labagnara M, Friedman M, et al. Glioblastoma: molecular pathways, stem cells and therapeutic targets. Cancers. 2015;7:538–555.
  • Takano S, Tsuboi K, Matsumura A, et al. Expression of the angiogenic factor thymidine phosphorylase in human astrocytic tumors. J Cancer Res Clin Oncol. 2000;126(3):145–152.
  • St Croix B, Rago C, Velculescu V, et al. Genes expressed in human tumor endothelium. Science. 2000;289(5482):1197–1202.
  • Zhou Y, Larsen PH, Hao C, et al. CXCR4 is a major chemokine receptor on glioma cells and mediates their survival. J Biol Chem. 2002;277(51):49481–49487.
  • Debinski W, Obiri NI, Powers SK, et al. Human glioma cells overexpress receptors for interleukin 13 and are extremely sensitive to a novel chimeric protein composed of interleukin 13 and pseudomonas exotoxin. Clin Cancer Res. 1995;1(11):1253–1258.
  • Desbaillets I, Diserens A, Tribolet N, et al. Upregulation of interleukin 8 by oxygen-deprived cells in glioblastoma suggests a role in leukocyte activation, chemotaxis, and angiogenesis. J Exp Med. 1997;186(8):1201–1212.
  • Kuppner MC, Van Meir E, Gauthier T, et al. Differential expression of the CD44 molecule in human brain tumours. Int J Cancer. 1992;50(4):572–577.
  • Knüpfer MM, Poppenborg H, Hotfilder M, et al. CD44 expression and hyaluronic acid binding of malignant glioma cells. Clin Exp Metastasis. 1999;17(1):81–86.
  • Yoshimura T, Teizo KJ. Chemokines and central nervous system malignancies. Chemokines Cancer. 1999;227–241. Humana Press.
  • Wu J, Zhao J, Zhang B, et al. Polyethylene glycol-polylactic acid nanoparticles modified with cysteine-arginine-glutamic acid-lysine-alanine fibrin-homing peptide for glioblastoma therapy by enhanced retention effect. Int J Nanomedicine. 2014;9:5261–5271.
  • Shu Q, Wong KK, Su JM, et al. Direct orthotopic transplantation of fresh surgical specimen preserves CD133+ tumor cells in clinically relevant mouse models of medulloblastoma and glioma. Stem Cells. 2008;26:1414–1424.
  • Anido J, Saez-Borderias A, Gonzalez-Junca A, et al. TGF-beta receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell. 2010;18:655–668.
  • Ortensi B, Setti M, Osti D, et al. Cancer stem cell contribution to glioblastoma invasiveness. Stem Cell Res Ther. 2013;4(1):18.
  • Wu D, Gao Y, Qi Y, et al. Peptide-based cancer therapy: opportunity and challenge. Cancer Lett. 2014;351:13–22.
  • Siyad MA, Vinod Kumar GS. Synthesis and characterization of linear and cyclic endothelin peptides on PEGylated poly(O-benzyl ether) dendrimeric supports. Polymer. 2015;67:80–91.
  • Siyad MA, Vinod Kumar GS. A class of linker free amphiphilic PEG grafted polymer support for linear and cyclic peptides. RSC Advances. 2014;4:60404–60408.
  • Siyad MA, Vinod Kumar GS. Synthetic evaluation of disulphide-bonded sarafotoxin on a poly(oxy ether) grafted dendrimeric poly(alkylamine) support for polymer assisted organic synthesis. Org Biomol Chem. 2013;11:4860–4870.
  • Lekha NK, Jagadeeshan S, Asha NS, et al. Evaluation of triblock copolymeric micelles of delta-valerolactone and poly (ethylene glycol) as a competent vector for doxorubicin delivery against cancer. J Nanobiotechnol. 2011;9:42.
  • Jisha JP, Arun Kumar TT, Ruby John A, et al. Folic acid conjugated cross-linked acrylic polymer (FA-CLAP) hydrogel for site specific delivery of hydrophobic drugs to cancer cells. J Nanobiotechnol. 2014;12:25.
  • Maeda H, Bharate GY, Daruwalla J. Polymeric drugs for efficient tumor-targeted drug delivery based on EPR-effect. Eur J Pharm Biopharm. 2009;71:409–419.
  • Li J, Feng L, Fan L, et al. Targeting the brain with PEG-PLGA nanoparticles modified with phage-displayed peptides. Biomaterials. 2011;32:4943–4950.
  • Yang ZZ, Li JQ, Wang ZZ, et al. Tumor-targeting dual peptides-modified cationic liposomes for delivery of siRNA and docetaxel to gliomas. Biomaterials. 2014;35:5226–5239.
  • Binétruy-Tournaire R, Demangel C, Malavaud B, et al. Identification of a peptide blocking vascular endothelial growth factor (VEGF)-mediated angiogenesis. EMBO J. 2000;19(7):1525–1533.
  • Yao H, Wang K, Wang Y, et al. Enhanced blood–brain barrier penetration and glioma therapy mediated by a new peptide modified gene delivery system. Biomaterials. 2015;37:345–352.
  • Hu Q, Gao X, Gu G, et al. Glioma therapy using tumor homing and penetrating peptide-functionalized PEG-PLA nanoparticles loaded with paclitaxel. Biomaterials. 2013;34:5640–5650.
  • Alvarez-Erviti L, Seow Y, Yin H, et al. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nature Biotechnol. 2011;29:341–345.
  • Chen L, Zhang J, Feng Y, et al. MiR-410 regulates MET to influence the proliferation and invasion of glioma. Int J Biochem Cell Biol. 2012;44:1711–1717.
  • Xia H, Qi Y, Ng SS, et al. MicroRNA-146b inhibits glioma cell migration and invasion by targeting MMPs. Brain Res. 2009;1269:158–165.
  • Li Y, Wang Y, Yu L, et al. MiR-146b-5p inhibits glioma migration and invasion by targeting MMP16. Cancer Lett. 2013;339:260–269.
  • Simeoni F, Morris MC, Heitz F, et al. Insight into the mechanism of the peptide‐based gene delivery system MPG: implications for delivery of siRNA into mammalian cells. Nucleic Acids Res. 2003;31:2717–2724.
  • Zhang -X-X, Eden HS, Chen X. Peptides in cancer nanomedicine: drug carriers, targeting ligands and protease substrates. J Control Release. 2012;159:2–13.
  • Madani F, Lindberg S, Langel U, et al. Mechanisms of cellular uptake of cell-penetrating peptides. J Biophys. 2011;2011. doi:10.1155/2011/414729.
  • Wang B, Lv L, Wang Z, et al. Nanoparticles functionalized with Pep-1 as potential glioma targeting delivery system via interleukin 13 receptor α2-mediated endocytosis. Biomaterials. 2014;35(22):5897–5907.
  • Vives E, Schmidt J,A, Pelegrin A. Cell-penetrating and cell-targeting peptides in drug delivery. Biochim Biophys Acta. 2008;1786:126–138.
  • Ali IU, Chen X. Penetrating the blood–brain barrier: promise of novel nanoplatforms and delivery vehicles. ACS Nano. 2015;9(10):9470–9474.
  • Gao H, Yang Z, Zhang S, et al. Glioma-homing peptide with a cell-penetrating effect for targeting delivery with enhanced glioma localization, penetration and suppression of glioma growth. J Control Release. 2013;172:921–928.
  • Wang J, Lei Y, Xie C, et al. Retro-inverso CendR peptide-mediated polyethyleneimine for intracranial glioblastoma-targeting gene therapy. Bioconjug Chem. 2014;25:414–423.
  • Gautam A, Sharma M, Vir P, et al. Identification and characterization of novel protein-derived arginine-rich cell-penetrating peptides. Eur J Pharm Biopharm. 2015;89:93–106.
  • von Wronski MA, Raju N, Pillai R, et al. Tuftsin binds neuropilin-1 through a sequence similar to that encoded by exon 8 of vascular endothelial growth factor. J Biol Chem. 2006;281(9):5702–5710.
  • Najjar VA, Nishioka K. Tuftsin’: a natural phagocytosis stimulating peptide. Nature. 1970;228(5272):672–673.
  • Teesalu T, Sugahara KN, Kotamraju VR, et al. C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc Natl Acad Sci. 2009;106(38):16157–16162.
  • Roth L, Agemy L, Kotamraju VR, et al. Transtumoral targeting enabled by a novel neuropilin-binding peptide. Oncogene. 2012;31(33):3754–3763.
  • Mollinedo F, Gajate C. Microtubules, microtubule-interfering agents and apoptosis. Apoptosis. 2003;8:413–450.
  • Jordan MA, Kamath K. How do microtubule-targeted drugs work? An overview. Curr Cancer Drug Tar. 2007;7:730–742.
  • Bolhassani A. Potential efficacy of cell-penetrating peptides for nucleic acid and drug delivery in cancer. Biochim Biophys Acta. 2011;1816:232–246.
  • Fialho AM, Salunkhe P, Manna S, et al. Glioblastoma multiforme: novel therapeutic approaches. ISRN Neurology. 2012;2012:642345.
  • Gao H, Qian J, Cao S, et al. Precise glioma targeting of and penetration by aptamer and peptide dual-functioned nanoparticles. Biomaterials. 2012;33:5115–5123.
  • Ruan S, Yuan M, Zhang L, et al. Tumor microenvironment sensitive doxorubicin delivery and release to glioma using angiopep-2 decorated gold nanoparticles. Biomaterials. 2015;37:425–435.
  • Teng Y, Girvan AC, Casson LK, et al. AS1411 alters the localization of a complex containing protein arginine methyltransferase 5 and nucleolin. Cancer Res. 2007;67:10491–10500.
  • Gao H, Zhang S, Cao S, et al. Angiopep-2 and activatable cell-penetrating peptide dual-functionalized nanoparticles for systemic glioma-targeting delivery. Mol Pharm. 2014;11:2755–2763.
  • Liu Y, Mei L, Yu Q, et al. Multifunctional tandem peptide modified paclitaxel-loaded liposomes for the treatment of vasculogenic mimicry and cancer stem cells in malignant glioma. ACS Appl Mater Interfaces. 2015;7(30):16792–16801.
  • Shi K, Long Y, Xu C, et al. Liposomes combined an integrin αvβ3-specific vector with pH-responsible cell-penetrating property for highly effective antiglioma therapy through the blood–brain barrier. ACS Appl Mater Interfaces. 2015;7(38):21442–21454.
  • Zhang B, Zhang Y, Liao Z, et al. UPA-sensitive ACPP-conjugated nanoparticles for multi-targeting therapy of brain glioma. Biomaterials. 2015;36:98–109.
  • Han L, Zhang A, Wang H, et al. Tat-BMPs-PAMAM conjugates enhance therapeutic effect of small interference RNA on U251 glioma cells in vitro and in vivo. Hum Gene Ther. 2010;21:417–426.
  • Debin JA, Maggio JE, Strichartz GR. Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion. Am J Physiol. 1993;264:C361–C369.
  • Mamelak AN, Jacoby DB. Targeted delivery of antitumoral therapy to glioma and other malignancies with synthetic chlorotoxin (TM-601). Expert Opin Drug Deliv. 2007;2:175–186.
  • Veiseh O, Sun C, Fang C, et al. Specific targeting of brain tumors with an optical/magnetic resonance imaging nanoprobe across the blood-brain barrier. Cancer Res. 2009;69:6200–6207.
  • Huang R, Ke W, Han L, et al. Targeted delivery of chlorotoxin-modified DNA-loaded nanoparticles to glioma via intravenous administration. Biomaterials. 2011;32:2399–2406.
  • Graf N, Mokhtari TE, Papayannopoulos IA, et al. Platinum (IV)-chlorotoxin (CTX) conjugates for targeting cancer cells. J Inorg Biochem. 2012;110:58–63.
  • Ho IA, Hui KM, Lam PY. Isolation of peptide ligands that interact specifically with human glioma cells. Peptides. 2010;31:644–650.
  • Xu LW, Chow KK, Lim M, et al. Current vaccine trials in glioblastoma: a review. J Immunol Res. 2014;2014:796856.
  • Schuster J, Lai RK, Recht LD, et al. A phase II, multicenter trial of rindopepimut (CDX-110) in newly diagnosed glioblastoma: the ACT III study. Neuro Oncol. 2015;17(6):854–861.
  • Dutoit V, Mende CH, Hilf N, et al. Exploiting the glioblastoma peptidome to discover novel tumour-associated antigens for immunotherapy. Brain. 2012;135:1042–1054.
  • Terasaki M, Shibui S, Narita Y, et al. Phase I trial of a personalized peptide vaccine for patients positive for human leukocyte antigen–A24 with recurrent or progressive glioblastoma multiforme. J Clin Oncol. 2011;29:337–344.
  • Bernatchez C, Zhu K, Li Y, et al. Altered decamer and nonamer from an HLA-A0201-restricted epitope of survivin differentially stimulate T-cell responses in different individuals. Vaccine. 2011;29:3021–3030.
  • Pollack IF, Jakacki RI, Butterfield LH, et al. Antigen-specific immune responses and clinical outcome after vaccination with glioma-associated antigen peptides and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in children with newly diagnosed malignant brainstem and nonbrainstem gliomas. J Clin Oncol. 2014;32:2050–2058.
  • Boockvar J, Bodhinayake I, Brooks C, et al. Initiation of clinical studies with SL-701, a synthetic multi-peptide vaccine with enhanced immunostimulatory properties targeting multiple glioma-associated antigens, in adults with first recurrence of glioblastoma. Neuro Oncol. 2014;2014:16.
  • Zhang B, Sun X, Mei H, et al. LDLR-mediated peptide-22-conjugated nanoparticles for dual-targeting therapy of brain glioma. Biomaterials. 2013;34:9171–9182.
  • Zhang B, Wang H, Liao Z, et al. EGFP-EGF1-conjugated nanoparticles for targeting both neovascular and glioma cells in therapy of brain glioma. Biomaterials. 2014;35:4133–4145.
  • Chung EJ, Cheng Y, Morshed R, et al. Fibrin-binding, peptide amphiphile micelles for targeting glioblastoma. Biomaterials. 2014;35:1249–1256.
  • Zhan C, Li B, Hu L, et al. Micelle‐based brain‐targeted drug delivery enabled by a nicotine acetylcholine receptor ligand. Angew Chem Int Ed Engl. 2011;50:5482–5485.
  • Burgo LSD, Hernández RM, Orive G, et al. Nanotherapeutic approaches for brain cancer management. Nanomedicine. 2014;10:905–919.
  • Wei X, Zhan C, Chen X, et al. Retro-inverso isomer of angiopep-2: a stable d-peptide ligand inspires brain-targeted drug delivery. Mol Pharm. 2014;11:3261–3268.
  • Diwan M, Tafaghodi M, Samuel J. Enhancement of immune responses by co-delivery of a CpG oligodeoxynucleotide and tetanus toxoid in biodegradable nanospheres. J Control Release. 2002;85:247–262.
  • Uto T, Wang X, Sato K, et al. Targeting of antigen to dendritic cells with poly(gamma-glutamic acid) nanoparticles induces antigen-specific humoral and cellular immunity. J Immunol. 2007;178:2979–2986.
  • Zhang Z, Tongchusak S, Mizukami Y, et al. Induction of anti-tumor cytotoxic T cell responses through PLGA-nanoparticle mediated antigen delivery. Biomaterials. 2011;32:3666–3678.
  • Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol. 2010;10:787–796.
  • Finocchiaro G, Pellegatta S. Immunotherapy with dendritic cells loaded with glioblastoma stem cells: from preclinical to clinical studies. Cancer Immunol Immunother. 2016;65(1):101–109.
  • Hurtado–Alvarado G, Cabañas–Morales AM, Gómez–Gónzalez B. Pericytes: brain-immune interface modulators. Front Integr Neurosci. 2013;7:80.
  • Wilson TA, Karajannis MA, Harter DH. Glioblastoma multiforme: state of the art and future therapeutics. Surg Neurol Int. 2014;5:64.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.