226
Views
1
CrossRef citations to date
0
Altmetric
Research Article

The Role of Disulfide Bonds in Structure and Activity of Chlorotoxin

, , , &
Pages 1617-1628 | Published online: 18 Nov 2014

References

  • Debin JA , MaggioJE, StrichartzGR. Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion. Am. J. Physiol.264 (2 Pt 1), C361–C369 (1993).
  • Lyons SA , O'NealJ, SontheimerH. Chlorotoxin, a scorpion-derived peptide, specifically binds to gliomas and tumors of neuroectodermal origin. Glia39 (2), 162–173 (2002).
  • Jacoby DB , DyskinE, YalcinMet al. Potent pleiotropic anti-angiogenic effects of TM601, a synthetic chlorotoxin peptide. Anticancer Res.30 (1), 39–46 (2010).
  • Soroceanu L , GillespieY, KhazaeliMB, SontheimerH. Use of chlorotoxin for targeting of primary brain tumors. Cancer Res.58 (21), 4871–4879 (1998).
  • Ullrich N , GillespieGY, SontheimerH. Human astrocytoma cells express a unique chloride current. Neuroreport7 (5), 1020–1024 (1996).
  • Deshane J , GarnerCC, SontheimerH. Chlorotoxin inhibits glioma cell invasion via matrix metalloproteinase-2. J. Biol. Chem.278 (6), 4135–4144 (2003).
  • Kesavan K , RatliffJ, JohnsonEWet al. Annexin A2 is a molecular target for TM601, a peptide with tumor-targeting and anti-angiogenic effects. J. Biol. Chem.285 (7), 4366–4374 (2010).
  • Stroud MR , HansenSJ, OlsonJM. In vivo bio-imaging using chlorotoxin-based conjugates. Curr. Pharm. Des.17 (38), 4362–4371 (2011).
  • Veiseh M , GabikianP, BahramiSBet al. Tumor paint: a chlorotoxin:Cy5.5 bioconjugate for intraoperative visualization of cancer foci. Cancer Res.67 (14), 6882–6888 (2007).
  • Kovar JL , CurtisE, OthmanSF, SimpsonMA, OliveDM. Characterization of IRDye 800CW chlorotoxin as a targeting agent for brain tumors. Anal. Biochem.440 (2), 212–219 (2013).
  • Hockaday DC , ShenS, FiveashJet al. Imaging glioma extent with 131I-TM-601. J. Nucl. Med.46 (4), 580–586 (2005).
  • Mamelak AN , RosenfeldS, BucholzRet al. Phase I single-dose study of intracavitary-administered iodine-131-TM-601 in adults with recurrent high-grade glioma. J. Clin. Oncol.24 (22), 3644–3650 (2006).
  • Costa PM , CardosoAL, MendoncaLSet al. Tumor-targeted chlorotoxin-coupled nanoparticles for nucleic acid delivery to glioblastoma cells: a promising system for glioblastoma treatment. Mol. Ther. Nucleic Acids2, e100 (2013).
  • Graf N , MokhtariTE, PapayannopoulosIA, LippardSJ. Platinum(IV)-chlorotoxin (CTX) conjugates for targeting cancer cells. J. Inorg. Biochem.110, 58–63 (2012).
  • Akcan M , StroudMR, HansenSJet al. Chemical re-engineering of chlorotoxin improves bioconjugation properties for tumor imaging and targeted therapy. J. Med. Chem.54 (3), 782–787 (2011).
  • Lippens G , NajibJ, WodakSJ, TartarA. NMR sequential assignments and solution structure of chlorotoxin, a small scorpion toxin that blocks chloride channels. Biochemistry34 (1), 13–21 (1995).
  • Daly NL , CraikDJ. Bioactive cystine knot proteins. Curr. Opin. Chem. Biol.15 (3), 362–368 (2011).
  • Garcia AE , CamareroJA. Biological activities of natural and engineered cyclotides, a novel molecular scaffold for peptide-based therapeutics. Curr. Mol. Pharmacol.3 (3), 153–163 (2010).
  • Wong CT , RowlandsDK, WongCHet al. Orally active peptidic bradykinin B1 receptor antagonists engineered from a cyclotide scaffold for inflammatory pain treatment. Angew. Chem. Int. Ed. Engl.51 (23), 5620–5624 (2012).
  • Gongora-Benitez M , Tulla-PucheJ, AlbericioF. Multifaceted roles of disulfide bonds. Peptides as therapeutics. Chem. Rev.114 (2), 901–926 (2014).
  • Colgrave ML , CraikDJ. Thermal, chemical and enzymatic stability of the cyclotide kalata B1: the importance of the cyclic cystine knot. Biochemistry43 (20), 5965–5975 (2004).
  • Wang CK , HuSH, MartinJLet al. Combined X-ray and NMR analysis of the stability of the cyclotide cystine knot fold that underpins its insecticidal activity and potential use as a drug scaffold. J. Biol. Chem.284 (16), 10672–10683 (2009).
  • Chan LY , ZhangVM, HuangYHet al. Cyclization of the antimicrobial peptide gomesin with native chemical ligation: influences on stability and bioactivity. Chembiochem14 (5), 617–624 (2013).
  • Zhu Q , LiangS, MartinL, GaspariniS, MenezA, VitaC. Role of disulfide bonds in folding and activity of leiurotoxin I: just two disulfides suffice. Biochemistry41 (38), 11488–11494 (2002).
  • Drakopoulou E , VizzavonaJ, NeytonJet al. Consequence of the removal of evolutionary conserved disulfide bridges on the structure and function of charybdotoxin and evidence that particular cysteine spacings govern specific disulfide bond formation. Biochemistry37 (5), 1292–1301 (1998).
  • Colgrave ML , PothAG, KaasQ, CraikDJ. A new “era” for cyclotide sequencing. Biopolymers94 (5), 592–601 (2010).
  • Chan LY , GunasekeraS, HenriquesSTet al. Engineering pro-angiogenic peptides using stable, disulfide-rich cyclic scaffolds. Blood118 (25), 6709–6717 (2011).
  • Conibear AC , RosengrenKJ, DalyNL, HenriquesST, CraikDJ. The cyclic cystine ladder in theta-defensins is important for structure and stability, but not antibacterial activity. J. Biol. Chem.288 (15), 10830–10840 (2013).
  • Aboye TL , ClarkRJ, BurmanR, RoigMB, CraikDJ, GoranssonU. Interlocking disulfides in circular proteins: toward efficient oxidative folding of cyclotides. Antioxid. Redox Signal.14 (1), 77–86 (2011).
  • Greenfield NJ . Using circular dichroism spectra to estimate protein secondary structure. Nat. Protoc.1 (6), 2876–2890 (2006).
  • Sabatier JM , LecomteC, MabroukKet al. Synthesis and characterization of leiurotoxin I analogs lacking one disulfide bridge: evidence that disulfide pairing 3–21 is not required for full toxin activity. Biochemistry35 (33), 10641–10647 (1996).
  • Vlieghe P , LisowskiV, MartinezJ, KhrestchatiskyM. Synthetic therapeutic peptides: science and market. Drug Discov. Today15 (1–2), 40–56 (2010).
  • Clark RJ , FischerH, DempsterLet al. Engineering stable peptide toxins by means of backbone cyclization: stabilization of the alpha-conotoxin MII. Proc. Natl Acad. Sci. USA102 (39), 13767–13772 (2005).
  • Clark RJ , JensenJ, NevinST, CallaghanBP, AdamsDJ, CraikDJ. The engineering of an orally active conotoxin for the treatment of neuropathic pain. Angew. Chem. Int. Ed. Engl.49 (37), 6545–6548 (2010).
  • Jia X , KwonS, WangCIet al. Semienzymatic cyclization of disulfide-rich peptides using Sortase A. J. Biol. Chem.289 (10), 6627–6638 (2014).
  • Borra R , CamareroJA. Recombinant expression of backbone-cyclized polypeptides. Biopolymers100 (5), 502–509 (2013).
  • Halai R , CallaghanB, DalyNL, ClarkRJ, AdamsDJ, CraikDJ. Effects of cyclization on stability, structure and activity of alpha-conotoxin RgIA at the alph9alpha10 nicotinic acetylcholine receptor and GABA(B) receptor. J. Med. Chem.54 (19), 6984–6992 (2011).
  • Lovelace ES , GunasekeraS, AlvarmoCet al. Stabilization of alpha-conotoxin AuIB: influences of disulfide connectivity and backbone cyclization. Antioxid. Redox Signal.14 (1), 87–95 (2011).
  • Wang CK , GruberCW, CemazarMet al. Molecular grafting onto a stable framework yields novel cyclic peptides for the treatment of multiple sclerosis. ACS. Chem. Biol.9 (1), 156–163 (2014).
  • Ji Y , MajumderS, MillardMet al. In vivo activation of the p53 tumor suppressor pathway by an engineered cyclotide. J. Am. Chem. Soc.135 (31), 11623–11633 (2013).

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.