Clathrin-mediated entry and cellular localization of chlorotoxin in human glioma

Cancer Cell International

Volumn 11, Issue , 2011, Pages

  Wiranowska, Marzenna ^a   Colina, Lucrecia O ^a   Johnson, Joseph O ^b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMILORIDE; BETA ACTIN; CHLOROTOXIN; CHLORPROMAZINE; CLATHRIN; FILIPIN; SCORPION VENOM; TM 601; UNCLASSIFIED DRUG;

ARTICLE; ASTROCYTE; CAVEOLA; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DRUG TUMOR LEVEL; ENDOCYTOSIS; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; PINOCYTOSIS; SKIN FIBROBLAST; TRANS GOLGI NETWORK;

EID: 80051582609     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/1475-2867-11-27     Document Type: Article

References (34)

1. Gelly JC, Gracy J, Kaas Q, Le-Nguyen D, Heitz A, Chiche L. The KNOTTIN website and database: a new information system dedicated to the knottin scaffold. Nucleic Acid Res 2004, 32:D156-D159. 10.1093/nar/gkh015, 308750, 14681383.
2. 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:C361-369.
3. Deshane J, Garner CC, Sontheimer H. Chlorotoxin inhibits glioma cell invasion via matrix metalloproteinase-2. J Biol Chem 2003, 278:4135-4144. 10.1074/jbc.M205662200, 12454020.
4. McFerrin MB, Sontheimer H. A role for ion channels in glioma cell invasion. Neuron Glia Biol 2006, 2:39-49. 1389710, 16520829.
5. Jacoby DB, Dyskin E, Yalcin M, Kesavan K, Dahlberg W, Ratliff J, Johnson EW, Mousa SA. Potent Pleiotropic Anti-angiogenic Effects of TM601, a Synthetic Chlorotoxin Peptide. Anticancer Res 2010, 30:39-46.
6. Veiseh M, Gabikian P, Bahram S-B, Veish O, Zhang M, Hackman R, Ravanpay AC, Stroud MR, Kusuma Y, Hansen SJ, Kwok D, Munoz NM, Sze RW, Grady WM, Greenberg NM, Ellenbogen RG, Olson JM. Tumor paint: Chlorotoxin: Cy5.5 bioconjugate for intraoperative visualization of cancer foci. Cancer Res 2007, 67:6882-6888. 10.1158/0008-5472.CAN-06-3948, 17638899.
7. Meng XX, Wan JQ, Jing M, Zhao SG, Cai W, Liu EZ. Specific targeting of gliomas with multifunctional superparamagnetic iron oxide nanoparticles optical and magnetic resonance imaging contrast agents. Acta Pharmacol Sin 2007, 28:2019-2026. 10.1111/j.1745-7254.2007.00661.x, 18031618.
8. Sun C, Veiseh O, Gunn J, Fang C, Hansen S, Lee D, Sze R, Ellenbogen RG, Olson J, Zhang M. In vivo MRI detection of gliomas by chlorotoxin-conjugated superparamagnetic nanoprobes. Small 2008, 4:372-379. 10.1002/smll.200700784, 2692358, 18232053.
9. Veiseh O, Kievit FM, Gunn JW, Ratner BD, Zhang M. A ligand-mediated nanovector for targeted gene delivery and transfection in cancer cells. Biomaterials 2009, 30:649-657. 10.1016/j.biomaterials.2008.10.003, 2709815, 18990439.
10. Shen S, Khazaeli MB, Gillespie GY, Alvarez VL. Radiation dosimetry of 131-I-chlorotoxin radiotherapy in glioma-bearing mice. J Neuro-Oncol 2005, 71:113-119.
11. Veiseh O, Gunn JW, Kievit FM, Sun C, Fang C, Lee JSH, Zhang M. Inhibition of tumor-cell invasion with chlorotoxin-bound supermagnetic nanoparticles. Small 2009, 5:256-264. 2692352, 19089837.
12. Gibbin TE, Senzer N, Raizer JJ, Shen J, Nabors LB, Wiranowska M, Fiveash JB. A phase I evaluation of intravenous (IV) 131I-chlorotoxin delivery to solid peripheral and intracranial tumors. J Clin Oncol 2009, 27:e14507.
13. Mamelak AN, Rosenfeld S, Bucholz R, Raubitschek A, Nabors LB, Fiveash JB, Shen S, Khazaeli MB, Colcher D, Liu A, Osman M, Guthrie B, Schade-Bijur S, Hablitz DM, Alvarez VL, Gonda MA. Phase I single-dose study of intracavitary-administered iodine-131I-TM-601 in adults with recurrent high-grade glioma. J Clin Oncol 2006, 24:3644-3650. 10.1200/JCO.2005.05.4569, 16877732.
14. Mamelak AN, Jacoby DB. Targeted delivery of antitumoral therapy to glioma and other malignancies with synthetic chlorotoxin (TM-601). Expert Opin Drug Deliv 2007, 4:175-186. 10.1517/17425247.4.2.175, 17335414.
15. Lyons SA, O'Neal J, Sontheimer H. Chlorotoxin, a scorpion-derived peptide, specifically binds to gliomas and tumors of neuroectodermal origin. Glia 2002, 39:162-173. 10.1002/glia.10083, 12112367.
16. Kesavan K, Ratliff J, Johnson EW, Dahlberg W, Asara JM, Misra P, Frangioni JV, Jacoby DB. Annexin A2 is a molecular target for TM601, a peptide with tumor-targeting and anti-angiogenic effects. J Biol Chem 2010, 285:4366-4374. 10.1074/jbc.M109.066092, 2836041, 20018898.
17. Orlandi PA, Fishman PH. Filipin-dependent inhibition of cholera toxin: Evidence for toxin internalization and activation through caveolae-like domains. J Cell Biol 1998, 141:905-915. 10.1083/jcb.141.4.905, 2132770, 9585410.
18. Anderson RG, Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 2002, 296:1821-1825. 10.1126/science.1068886, 12052946.
19. Khalil IA, Kogure K, Futaki S, Harashima H. High density of octaarginine stimulates macropinocytosis leading to efficient intracellular trafficking for gene experession. J Biol Chem 2006, 281:3544-3551.
20. Chen C-L, Hou W-H, Liu I-H, Hsiao G, Huang SS, Huang JS. Inhibitors of clathrin-dependent endocytosis enhance TGFβ signaling and responses. J Cell Sci 2009, 122:1863-1871. 10.1242/jcs.038729, 2684837, 19461075.
21. Cortese K, Sahores M, Madsen CD, Tacchetti C, Blasi F. Clathrin and LRP-1-independent constitutive endocytosis and recycling of uPAR. PLoS ONE 2008, 3(11):e3730. 10.1371/journal.pone.0003730, 2579578, 19008962.
22. Foster LJ, De Hoog CL, Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci USA 2003, 100:5813-5818. 10.1073/pnas.0631608100, 156283, 12724530.
23. Pho MT, Ashok A, Atwood WJ. JC virus enters human glial cells by clathrin-dependent receptor-mediated endocytosis. J Virology 2000, 74:2288-2292. 10.1128/JVI.74.5.2288-2292.2000, 111710, 10666259.
24. Jin AJ, Nossal R. Topological mechanisms involved in the formation of clathrin-coated Vesicles. Biophysical J 1993, 65:1523-1537.
25. Schnitzer JE, Oh P, Pinney E, Allard J. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol 1994, 127:1217-1232. 10.1083/jcb.127.5.1217, 2120262, 7525606.
26. Bellve KD, Leonard D, Standley C, Lifshitz LM, Tuft RA, Hayakawa A, Corvera S, Fogarty KE. Plasma membrane domains specialized for clathrin-mediated endocytosis in primary cells. J Biol Chem 2006, 281:16139-16146. 10.1074/jbc.M511370200, 16537543.
27. Sofer A, Futerman AH. Cathionic amphiphilic drugs inhibit the internalization of cholera toxin to the Golgi apparatus and subsequent elevation of cyclic AMP. J Biol Chem 1995, 270:12117-12122. 10.1074/jbc.270.20.12117, 7744860.
28. Poupon V, Girard M, Legendre-Guillemin V, Thomas S, Bourbonniere L, Philie J, Bright NA, McPherson PS. Clathrin light chains function in mannose phosphate receptor trafficking via regulation of actin assembly. Proc Natl Acad Sci USA 2008, 105:168-173. 10.1073/pnas.0707269105, 2224180, 18165318.
29. Puri V, Watanabe R, Singh RD, Dominguez M, Brown JC, Wheatley CL, Marks DL, Pagano RE. Clathrin-dependent and independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways. J Cell Biol 2001, 154:535-547. 10.1083/jcb.200102084, 2196434, 11481344.
30. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 2008, 15:209-219. 10.1016/j.devcel.2008.06.012, 18694561.
31. DiPaola M, Keith CH, Feldman D, Tycko B, Maxfield FR. Loss of α2 macroglobulin and epidermal growth factor surface binding induced by phenothiazines and naphthalene sulfonamides. J Cell Physiol 1984, 118:193-202. 10.1002/jcp.1041180212, 6319437.
32. Wang LH, Rothenberg KG, Anderson RG. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 1993, 123:1107-1117. 10.1083/jcb.123.5.1107, 2119875, 8245121.
33. Seaman MN, Ball CL, Robinson MS. Targeting and mistargeting of plasma membrane adaptors in vitro. J Cell Biol 1993, 123:1093-1105. 10.1083/jcb.123.5.1093, 2119871, 8245120.
34. Mori M, Itabe H, Higashi Y, Fujimoto Y, Shiomi M, Yoshizumi M, Ouchi Y, Takano T. Foam cell formation containing lipid droplets enriched with free cholesterol by hyperlipidemic serum. J Lipid Res 2001, 42:1771-1781.