Binding, transcytosis and biodistribution of anti-PECAM-1 iron oxide nanoparticles for brain-targeted delivery

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Dan, Mo ^a,b,d   Cochran, David B ^c   Yokel, Robert A ^a,b   Dziubla, Thomas D ^c  

^a University of Kentucky   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d NATIONAL INSTITUTES FOR FOOD AND DRUG CONTROL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CD31 ANTIGEN IRON OXIDE NANOPARTICLE; HEPARIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G IRON OXIDE NANOPARTICLE; NUCLEAR MAGNETIC RESONANCE IMAGING AGENT; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; UNCLASSIFIED DRUG; FERRIC ION; FERRIC OXIDE; METAL NANOPARTICLE; MONOCLONAL ANTIBODY; PROTEIN BINDING;

ANALYTIC METHOD; ANALYTICAL PARAMETERS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BLOOD ANALYSIS; BLOOD BRAIN BARRIER; BRAIN; BRAIN PARENCHYMA; CAPILLARY DEPLETION METHOD; CELL IMMORTALIZATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISSOCIATION CONSTANT; DRUG ACCUMULATION; DRUG BINDING; DRUG BRAIN LEVEL; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG TARGETING; DRUG TISSUE LEVEL; DRUG TRANSPORT; HUMAN; HUMAN CELL; IMMUNOSPECIFICITY INDEX; IN VITRO STUDY; IN VIVO STUDY; LIVER LEVEL; LUNG; MALE; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PARTICLE SIZE; PROTEIN TRANSPORT; RAT; SPLEEN; SPRAGUE DAWLEY RAT; TRANSCYTOSIS; ANIMAL; CELL LINE; CHEMISTRY; ENDOTHELIUM CELL; IMMUNOLOGY; METABOLISM; TISSUE DISTRIBUTION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD31; BLOOD-BRAIN BARRIER; BRAIN; CELL LINE; ENDOTHELIAL CELLS; FERRIC COMPOUNDS; HUMANS; IMMUNOGLOBULIN G; MALE; METAL NANOPARTICLES; PROTEIN BINDING; RATS; TISSUE DISTRIBUTION; TRANSCYTOSIS;

EID: 84894272589     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081051     Document Type: Article

References (52)

1. Silva AC, Oliveira TR, Mamani JB, Malheiros SMF, Malavolta L, et al. (2011) Application of hyperthermia induced by superparamagnetic iron oxide nanoparticles in glioma treatment. Int J Nanomedicine 6: 591-603.
2. Bhaskar S, Tian F, Stoeger T, Kreyling W, de la Fuente JM, et al. (2010) Multifunctional Nanocarriers for diagnostics, drug delivery and targeted treatment across blood-brain barrier: perspectives on tracking and neuroimaging. Part Fibre Toxicol 7: 3.
3. Weinstein JS, Varallyay CG, Dosa E, Gahramanov S, Hamilton B, et al. (2010) Superparamagnetic iron oxide nanoparticles: diagnostic magnetic resonance imaging and potential therapeutic applications in neurooncology and central nervous system inflammatory pathologies, a review. J Cerebr Blood F Met 30: 15-35.
4. Wankhede M, Bouras A, Kaluzova M, Hadjipanayis CG (2012) Magnetic nanoparticles: an emerging technology for malignant brain tumor imaging and therapy. Expert Rev Clin Pharmacol 5: 173-186.
5. Hu JM, Qian YF, Wang XF, Liu T, Liu SY (2012) Drug-Loaded and superparamagnetic iron oxide nanoparticle surface-embedded amphiphilic block copolymer micelles for integrated chemotherapeutic drug delivery and MR imaging. Langmuir 28: 2073-2082.
6. Dilnawaz F, Singh A, Mewar S, Sharma U, Jagannathan NR, et al. (2012) The transport of non-surfactant based paclitaxel loaded magnetic nanoparticles across the blood brain barrier in a rat model. Biomaterials 33: 2936-2951.
7. Cole AJ, David AE, Wang J, Galbán CJ, Yang VC (2011) Magnetic brain tumor targeting and biodistribution of long-circulating PEG-modified, cross-linked starch-coated iron oxide nanoparticles. Biomaterials 32: 6291-6301.
8. Veiseh O, Sun C, Fang C, Bhattarai N, Gunn J, et al. (2009) Specific targeting of brain tumors with an optical/magnetic resonance imaging nanoprobe across the blood-brain barrier. Cancer Res 69: 6200-6207.
9. Bernacki J, Dobrowolska A, Nierwinska K, Malecki A (2008) Physiology and pharmacological role of the blood-brain barrier. Pharmacol Rep 60: 600-622.
10. Kenzaoui BH, Bernasconi CC, Hofmann H, Juillerat-Jeanneret L (2012) Evaluation of uptake and transport of ultrasmall superparamagnetic iron oxide nanoparticles by human brain-derived endothelial cells. Nanomedicine 7: 39-53.
11. Scherpereel A, Rome JJ, Wiewrodt R, Watkins SC, Harshaw DW, et al. (2002) Platelet-endothelial cell adhesion molecule-1-directed immunotargeting to cardiopulmonary vasculature. J Pharmacol Exp Ther 300: 777-786. (Pubitemid 34164979)
12. Wong D, Dorovini-Zis K (1996) Platelet/endothelial cell adhesion molecule-1 (PECAM-1) expression by human brain microvessel endothelial cells in primary culture. Brain Res 731: 217-220. (Pubitemid 26294927)
13. Kalinowska A, Losy J (2006) PECAM-1, a key player in neuroinflammation. Eur J Neurol 13: 1284-1290. (Pubitemid 44736636)
14. Ding BS, Dziubla T, Shuvaev VV, Muro S, Muzykantov VR (2006) Advanced drug delivery systems that target the vascular endothelium. Mol Interv 6: 98-112.
15. Muro S, Wiewrodt R, Thomas A, Koniaris L, Albelda SM, et al. (2003) A novel endocytic pathway induced by clustering endothelial ICAM-1 or PECAM-1. J Cell Sci 116: 1599-1609. (Pubitemid 36527505)
16. Muro S, Dziubla T, Qiu WN, Leferovich J, Cui X, et al. (2006) Endothelial targeting of high-affinity multivalent polymer nanocarriers directed to intercellular adhesion molecule 1. J Pharmacol Exp Ther 317: 1161-1169. (Pubitemid 43764121)
17. Frimpong RA, Hilt JZ (2010) Magnetic nanoparticles in biomedicine: synthesis, functionalization and applications. Nanomedicine (Lond) 5: 1401-1414.
18. Meenach SA, Hilt JZ, Anderson KW (2010) Poly(ethylene glycol)-based magnetic hydrogel nanocomposites for hyperthermia cancer therapy. Acta Biomater 6: 1039-1046.
19. Frimpong RA, Dou J, Pechan M, Hilt JZ (2010) Enhancing remote controlled heating characteristics in hydrophilic magnetite nanoparticles via facile co-precipitation. J Magn Magn Mater 322: 326-331.
20. Dan M, Scott DF, Hardy PA, Wydra RJ, Hilt JZ, et al. (2013) Block copolymer cross-linked nanoassemblies improve particle stability and biocompatibility of superparamagnetic iron oxide nanoparticles. Pharm Res 30: 552-561.
21. Salacinski PR, McLean C, Sykes JE, Clement-Jones VV, Lowry PJ (1981) Iodination of proteins, glycoproteins, and peptides using a solid-phase oxidizing agent, 1, 3, 4, 6-tetrachloro-3α, 6α-diphenyl glycoluril (Iodogen). Anal Biochem 117: 136-146. (Pubitemid 12211794)
22. Poller B, Gutmann H, Krahenbuhl S, Weksler B, Romero I, et al. (2008) The human brain endothelial cell line hCMEC/D3 as a human blood-brain barrier model for drug transport studies. J Neurochem 107: 1358-1368.
23. Carl SM, Lindley DJ, Couraud PO, Weksler BB, Romero I, et al. (2010) ABC and SLC transporter expression and pot substrate characterization across the human CMEC/D3 blood-brain barrier cell Line. Mol Pharm 7: 1057-1068.
24. Weksler BB, Subileau EA, Perriere N, Charneau P, Holloway K, et al. (2005) Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 19: 1872-1874. (Pubitemid 41598779)
25. Papademetriou J, Garnacho C, Serrano D, Bhowmick T, Schuchman EH, et al. (2013) Comparative binding, endocytosis, and biodistribution of antibodies and antibody-coated carriers for targeted delivery of lysosomal enzymes to ICAM-1 versus transferrin receptor. J Inherit Metab Dis 36: 467-477.
26. Triguero D, Buciak J, Pardridge WM (1990) Capillary depletion method for quantification of blood-brain barrier transport of circulating peptides and plasma proteins. J Neurochem 54: 1882-1888.
27. Crossgrove JS, Allen DD, Bukaveckas BL, Rhineheimer SS, Yokel RA (2003) Manganese distribution across the blood-brain barrier. I. Evidence for carrier-mediated influx of managanese citrate as well as manganese and manganese transferrin. NeuroToxicology 24: 3-13. (Pubitemid 36091156)
28. Smith QR (1996) Brain perfusion systems for studies of drug uptake and metabolism in the central nervous system. Pharm Biotechnol 8: 285-307.
29. Nozinic D, Milic A, Mikac L, Ralic J, Padovan J, et al. (2010) Assessment of macrolide transport using PAMPA, Caco-2 and MDCKII-hMDR1 assays. Croat Chem Acta 83: 323-331.
30. Chacko AM, Nayak M, Greineder CF, Delisser HM, Muzykantov VR (2012) Collaborative enhancement of antibody binding to distinct PECAM-1 epitopes modulates endothelial targeting. PLoS One 7: e34958.
31. Yu YJ, Zhang Y, Kenrick M, Hoyte K, Luk W, et al. (2011) Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target. Sci Transl Med 3: 84ra44.
32. Dziubla TD, Shuvaev VV, Hong NK, Hawkins BJ, Madesh M, et al. (2008) Endothelial targeting of semi-permeable polymer nanocarriers for enzyme therapies. Biomaterials 29: 215-227. (Pubitemid 350017841)
33. Peng X-H, Qian X, Mao H, Wang AY (2008) Targeted magnetic iron oxide nanoparticles for tumor imaging and therapy. Int J nanomedicine 3: 311.
34. Jiang W, Xie H, Ghoorah D, Shang Y, Shi H, et al. (2012) Conjugation of functionalized SPIONs with transferrin for targeting and imaging brain glial tumors in rat model. PLoS One 7: e37376.
35. Corot C, Robert P, Idée J-M, Port M (2006) Recent advances in iron oxide nanocrystal technology for medical imaging. Adv Drug Delivery Rev 58: 1471-1504. (Pubitemid 44820503)
36. Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78: 857-902.
37. Hillaireau H, Couvreur P (2009) Nanocarriers' entry into the cell: relevance to drug delivery. Cell Mol Life Sci 66: 2873-2896.
38. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422: 37-44. (Pubitemid 36323287)
39. Chang J, Jallouli Y, Kroubi M, Yuan X-b, Feng W, et al. (2009) Characterization of endocytosis of transferrin-coated PLGA nanoparticles by the blood-brain barrier. Int J Pharmaceut 379: 285-292.
40. Minshall RD, Tiruppathi C, Vogel SM, Niles WD, Gilchrist A, et al. (2000) Endothelial cell-surface gp60 activates vesicle formation and trafficking via G(i)-coupled Src kinase signaling pathway. J Cell Biol 150: 1057-1070.
41. Hansen SH, Sandvig K, van Deurs B (1993) Clathrin and HA2 adaptors: effects of potassium depletion, hypertonic medium, and cytosol acidification. J Cell Biol 121: 61-72. (Pubitemid 23097362)
42. Garnacho C, Shuvaev V, Thomas A, McKenna L, Sun J, et al. (2008) RhoA activation and actin reorganization involved in endothelial CAM-mediated endocytosis of anti-PECAM carriers: critical role for tyrosine 686 in the cytoplasmic tail of PECAM-1. Blood 111: 3024-3033.
43. Wu DF, Kang YS, Bickel U, Pardridge WM (1997) Blood-brain barrier permeability to morphine-6-glucuronide is markedly reduced compared with morphine. Drug Metab Dispos 25: 768-771. (Pubitemid 27259979)
44. Jones AR, Shusta EV (2007) Blood-brain barrier transport of therapeutics via receptor-mediation. Pharm Res 24: 1759-1771. (Pubitemid 47206625)
45. Zhang P, Hu L, Yin Q, Zhang Z, Feng L, et al. (2012) Transferrin- conjugated polyphosphoester hybrid micelle loading paclitaxel for brain-targeting delivery: synthesis, preparation and in vivo evaluation. J Control Release 159: 429-434.
46. Shin SU, Friden P, Moran M, Olson T, Kang YS, et al. (1995) Transferrin-antibody fusion proteins are effective in brain targeting. Proc Natl Acad Sci U S A 92: 2820-2824.
47. Crowe A, Morgan EH (1992) Iron and transferrin uptake by brain and cerebrospinal fluid in the rat. Brain Res 592: 8-16.
48. Morgan EH, Moos T (2002) Mechanism and developmental changes in iron transport across the blood-brain barrier. Dev Neurosci 24: 106-113. (Pubitemid 36151440)
49. Shuvaev VV, Tliba S, Nakada M, Albelda SM, Muzykantov VR (2007) Platelet-endothelial cell adhesion molecule-1-directed endothelial targeting of superoxide dismutase alleviates oxidative stress caused by either extracellular or intracellular superoxide. J Pharmacol Exp Ther 323: 450-457. (Pubitemid 350005112)
50. Danilov SM, Gavrilyuk VD, Franke FE, Pauls K, Harshaw DW, et al. (2001) Lung uptake of antibodies to endothelial antigens: key determinants of vascular immunotargeting. Am J Physiol - Lung Cell Mol Physiol 280: L1335-L1347.
51. Kawabe T, Phi JH, Yamamoto M, Kim DG, Barfod BE, et al. (2012) Treatment of brain metastasis from lung cancer. Prog Neurol Surg 25: 148-155.
52. Kuang BH, Wen XZ, Ding Y, Peng RQ, Cai PQ, et al. (2013) The prognostic value of platelet endothelial cell adhesion molecule-1 in non-small-cell lung cancer patients. Med Oncol 30: 536.