Exosomes: Tunable nano vehicles for macromolecular delivery of transferrin and lactoferrin to specific intracellular compartment

Journal of Biomedical Nanotechnology

Volumn 12, Issue 5, 2016, Pages 1101-1114

  Malhotra, Himanshu ^a   Sheokand, Navdeep ^a   Kumar, Santosh ^a   Chauhan, Anoop S ^a   Kumar, Manoj ^a   Jakhar, Priyanka ^a   Boradia, Vishant M ^b   Raje, Chaaya I ^b   Raje, Manoj ^a  

^a INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

^b NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH NIPER   (India)

Author keywords

Delivery Vehicle; Exosome; GAPDH; Lactoferrin; Transferrin

Indexed keywords

CELLS; IRON RESEARCH; MACROMOLECULES; MAGNETIC LEVITATION VEHICLES; MAMMALS; MOLECULES; PROTEINS; VEHICLES;

DELIVERY VEHICLE; EXOSOME; GAPDH; LACTOFERRIN; TRANSFERRIN;

CYTOLOGY;

CARRIER PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LACTOFERRIN; TRANSFERRIN; DRUG CARRIER; IRON; MACROMOLECULE; NANOPARTICLE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOSOME; EXOSOME; INTRACELLULAR SPACE; LYSOSOME; MACROMOLECULE; NANODEVICE; NONHUMAN; PARTICLE SIZE; SUSPENSION; ZETA POTENTIAL; ANIMAL; CELL COMPARTMENTALIZATION; CHEMISTRY; CHO CELL LINE; CRICETULUS; DRUG DELIVERY SYSTEM; HAMSTER; HEPG2 CELL LINE; HUMAN; METABOLISM; RABBIT; ULTRASTRUCTURE;

ANIMALS; CELL COMPARTMENTATION; CHO CELLS; CRICETINAE; CRICETULUS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; ENDOSOMES; EXOSOMES; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HEP G2 CELLS; HUMANS; IRON; LACTOFERRIN; MACROMOLECULAR SUBSTANCES; NANOPARTICLES; RABBITS; TRANSFERRIN;

EID: 84962541986     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2016.2229     Document Type: Article

References (65)

1. A. Rosenkranz, A. Ulasov, T. Slastnikova, Y. Khramtsov, and A. Sobolev, Use of intracellular transport processes for targeted drug delivery into a specified cellular compartment. Biochemistry (Mosc.) 79, 928 (2014).
2. U. Testa (edn.), Proteins of Iron Metabolism, CRC Press Boca Raton, FL (2002).
3. N. C. Andrews, Forging a field: The golden age of iron biology. Blood 112, 219 (2008).
4. H. Li and Z. M. Qian, Transferrin/transferrin receptor-mediated drug delivery. Med. Res. Rev. 22, 225 (2002).
5. S. Oh, J. Rih, H. Kwon, S. Kim, and J. Yim, Lactoferrin as a gene delivery vehicle to hepatocytes, Exp. Mol. Med. 29, 111 (1997).
6. Z. M. Qian, H. Li, H. Sun, and K. Ho, Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway. Pharmacol. Rev. 54, 561 (2002).
7. K. B. Golla, C. Ahmed, and F. Kondapi, A target-specific oral formulation of doxorubicin-protein nanoparticles: Efficacy and safety in hepatocellular cancer. J. Cancer 4, 644 (2013).
8. M. Hong, S. Zhu, Y. Jiang, G. Tang, C. Sun, C. Fang, B. Shi, and Y. Pei, Novel anti-tumor strategy: PEG-hydroxycamptothecin conjugate loaded transferrin-PEG-nanoparticles. J. Control. Release 141, 22 (2010).
9. I. C. T. de Ilarduya and N. Düzgünes, Delivery of therapeutic nucleic acids via transferrin and transferrin receptors: Lipoplexes and other carriers. Expert Opin. Drug. Deliv. 10, 1583 (2013).
10. S. Tortorella and T. C. Karageinnis, Transferrin receptor-mediated endocytosis: A useful target for cancer therapy. J. Membrane. Biol. 247, 291 (2014).
11. L. M. Bareford and P. W. Swaan, Endocytic mechanisms for targeted drug delivery. Adv. Drug Deliv. Rev. 59, 748 (2007).
12. L. Rajendran, H. J. Knölker, and K. Simons, Subcellular targeting strategies for drug design and delivery. Nat. Rev. Drug Discov. 9, 29 (2010).
13. R. Mears, R. A. Craven, S. Hanrahan, N. Totty, C. Upton, S. L. Young, P. Patel, P. J. Selby, and R. E. Banks, Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics 4, 4019 (2004).
14. F. Raimondo, L. Morosi, C. Chinello, F. Magni, and M. Pitto, Advances in membranous vesicle and exosome proteomics improving biological understanDing and biomarker discovery. Proteomics 11, 709 (2011).
15. A. V. Vlassov, S. Magdaleno, R. Setterquist, and R. Conrad, Exosomes: Current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim. Biophys. Acta. 1820, 940 (2012).
16. C. Thery, M. Ostrowski, and E. Segura, Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581 (2009).
17. L. Zitvogel, A. Regnault, A. Lozier, J. Wolfers, C. Flament, D. Tenza, P. Ricciardi-Castagnoli, G. Raposo, and S. Amigorena, Eradication of established murine tumors using a novel cell-free vaccine: Dendritic cell derived exosomes. Nat. Med. 4, 594 (1998).
18. J. De Toro, L. Herschlik, C. Waldner, and C. Mongini, Emerging roles of exosomes in normal and pathological conditions: New insights for diagnosis and therapeutic applications. Front Immunol. 6, 203 (2015).
19. C. Frühbeis, D. Fröhlich, and EM. Krämer-Albers, Emerging roles of exosomes in neuron-glia communication. Front Physiol. 3, 119 (2012).
20. T. N. Bukong, F. Momen-Heravi, K. Kodys, S. Bala, and G. Szabo, Exosomes from Hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90. PLoS Pathog. 10, 10 (2014).
21. B. Fevrier, D. Vilette, F. Archer, D. Loew, W. Faigle, M. Vidal, H. Laude, and G. Raposo, Cells release prions in association with exosomes. Proc. Natl. Acad. Sci. USA 29, 9683 (2004).
22. S. C. Jang, O. Y. Kim, C. M. Yoon, D.-S. Choi, T.-Y. Roh, J. Park, J. Nilsson, J. L?otvall, Y.-K. Kim, and Y. S. Gho, Bioinspired exosome-mimetic nanovesicles for targeted delivery of chemotherapeutics to malignant tumors. ACS Nano. 7, 7698 (2013).
23. C. Escrevente, S. Keller, P. Altevogt, and J. Costa, Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 11, 108 (2011).
24. J. Griffiths and S. Shaw, Glyceraldehyde-phosphate dehydrogenase (total and isoenzyme activity) in the early diagnosis of myocardial infarction. Clin. Chem. 23, 245 (1977).
25. C. I. Raje, S. Kumar, A. Harle, J. S. Nanda, and M. Raje, The macrophage cell surface glyceraldehyde-3-phosphate dehydrogenase is a novel transferrin receptor. J. Biol. Chem. 282, 3252 (2007).
26. R. Yamaji, E. Chatani, N. Harada, K. Sugimoto, H. Inui, and Y. Nakano, Glyceraldehyde-3-phosphate dehydrogenase in the extracellular space inhibits cell spreading. Biochim. Biophys. Acta. 1726, 261 (2005).
27. N. Sheokand, S. Kumar, H. Malhotra, V. Tillu, C. I. Raje, and M. Raje, Secreted glyceraldehye-3-phosphate dehydrogenase is a multifunctional autocrine transferrin receptor for cellular iron acquisition. Biochim. Biophys. Acta 1830, 3816 (2013).
28. V. M. Boradia, H. Malhotra, J. S. Thakkar, V. A. Tillu, B. Vuppala, P. Patil, N. Sheokand, P. Sharma, A. S. Chauhan, and M. Raje, Mycobacterium tuberculosis acquires iron by cell-surface sequestration and internalization of human holo-transferrin. Nat. Commun. 5, 4730 (2014).
29. S. Kumar, N. Sheokand, M. A. Mhadeshwar, C. I. Raje, and M. Raje, Characterization of glyceraldehyde-3-phosphate dehydrogenase as a novel transferrin receptor. Int. J. Biochem. Cell Biol. 44, 189 (2012).
30. B. Modun, J. Morrissey, and P. Williams, The staphylococcal transferrin receptor: A glycolytic enzyme with novel functions. Trends Microbiol. 8, 231 (2000).
31. B. Modun and P. Williams, The staphylococcal transferrin-binDing protein is a cell wall glyceraldehyde-3-phosphate dehydrogenase. Infect. Immun. 67, 1086 (1999).
32. P. Rawat, S. Kumar, N. Sheokand, C. I. Raje, and M. Raje, The multifunctional glycolytic protein glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is a novel macrophage lactoferrin receptor. Biochem. Cell Biol. 90, 329 (2012).
33. N. Sheokand, H. Malhotra, S. Kumar, V. A. Tillu, A. S. Chauhan, C. I. Raje, and M. Raje, Moonlighting cell-surface GAPDH recruits apotransferrin to effect iron egress from mammalian cells. J. Cell Sci. 127, 4279 (2014).
34. S. Mathivanan and R. J. Simpson, ExoCarta: A compendium of exosomal proteins and RNA. Proteomics 9, 4997 (2009).
35. T. E.McGraw, L. Greenfield, and F. R. Maxfield, Functional expression of the human transferrin receptor cDNA in Chinese hamster ovary cells deficient in endogenous transferrin receptor. J. Cell Biol. 105, 207 (1987).
36. N. C. Edwards, Z. A. Hing, A. Perry, A. Blaisdell, D. B. Kopelman, R. Fathke, W. Plum, J. Newell, C. E. Allen, S. Geetha, A. Shapiro, C. Okunji, I. Kosti, N. Shomron, V. Grigoryan, T. M. Przytycka, Z. E. Sauna, R. Salari, Y. Mandel-Gutfreund, A. A. Komar, and C. Kimchi-Sarfaty, Characterization of coDing synonymous and nonsynonymous variants in ADAMTS13 using ex vivo and in silico approaches. PLoS One 7, e38864 (2012).
37. C. V. Harding, J. E. Heuser, and P. D. Stahl, Exosomes: Looking back three decades and into the future. J. Cell Biol. 200, 367 (2013).
38. S. A. A. Kooijmans, P. Vader, S. M. van Dommelen, W. W. van Solinge, and R. M. Schiffelers, Exosome mimetics: A novel class of drug delivery systems. Int. J. Nanomedicine 7, 1525 (2012).
39. H. C. Christianson, K. J. Svensson, T. H. van Kuppevelt, J.-P. Li, and M. Belting, Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc. Natl. Acad Sci. USA 110, 17380 (2013).
40. J. S. Schorey and S. Bhatnagar, Exosome function: From tumor immunology to pathogen biology. Traffic 9, 871 (2008).
41. V. M. Boradia, M. Raje, and C. I. Raje, Protein moonlighting in iron metabolism: Glyceraldehyde-3-phosphate dehydrogenase (GAPDH). Biochem. Soc. Trans. 42, 1796 (2014).
42. R. Johnstone, A. Bianchini, and K. Teng, Reticulocyte maturation and exosome release: Transferrin receptor containing exosomes shows multiple plasma membrane functions. Blood 74, 1844 (1989).
43. K. J. Svensson, H. C. Christianson, A. Wittrup, E. Bourseau-Guilmain, E. Lindqvist, L. M. Svensson, M. Mörgelin, and M. Belting, Exosome uptake depends on ERK1/2-heat shock protein 27 signaling and lipid raft-mediated endocytosis negatively regulated by caveolin-1. J. Biol. Chem. 288, 17713 (2013).
44. D. Feng, W. L. Zhao, Y. Y. Ye, X. C. Bai, R. Q. Liu, L. F. Chang, Q. Zhou, and S. F. Sui, Cellular internalization of exosomes occurs through phagocytosis. Traffic 11, 675 (2010).
45. A. Koshkaryev, A. Piroyan, and V. P. Torchilin, Increased apoptosis in cancer cells in vitro and in vivo by ceramides in transferrinmodified liposomes. Cancer Biol. Ther. 13, 50 (2012).
46. G. Vaidyanathan, D. J. Affleck, J. Li, P. Welsh, and M. R. Zalutsky, A polar substituent-containing acylation agent for the radioiodination of internalizing monoclonal antibodies: N-succinimidyl 4-guanidinomethyl-3-[131I] iodobenzoate ([131I] SGMIB). Bioconjug. Chem. 12, 428 (2001).
47. C. Admyre, S. M. Johansson, K. R. Qazi, J.-J. Filen, R. Lahesmaa, M. Norman, E. P. A. Neve, A. Scheynius, and S. Gabrielsson, Exosomes with immune modulatory features are present in human breast milk. J. Immunol. 179, 1969 (2007).
48. M. Gonzalez-Begne, B. Lu, X. Han, F. K. Hagen, A. R. Hand, J. E. Melvin, and J. R. Yates, Proteomic analysis of human parotid gland exosomes by multidimensional protein identification technology (MudPIT). J. Proteome. Res. 8, 1304 (2009).
49. M. W. Graner, O. Alzate, A. M. Dechkovskaia, J. D. Keene, J. H. Sampson, D. A. Mitchell, and D. D. Bigner, Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 23, 1541 (2009).
50. S. Mathivanan, J. W. E. Lim, B. J. Tauro, H. Ji, R. L. Moritz, and R. J. Simpson, Proteomics analysis of A33 immunoaffinitypurified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol. Cell Proteomics 9, 197 (2010).
51. T. Pisitkun, R.-F. Shen, and M. A. Knepper, Identification and proteomic profiling of exosomes in human urine. Proc. Natl. Acad. Sci. USA 101, 13368 (2004).
52. H. Valadi, K. Ekstrom, A. Bossios, M. Sjostrand, J. J. Lee, and J. O. Lotvall, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654 (2007).
53. S. I. Buschow, B. W. M. van Balkom, M. Aalberts, A. J. R. Heck, M. Wauben, and W. Stoorvogel, MHC class II-associated proteins in B-cell exosomes and potential functional implications for exosome biogenesis. Immunol. Cell Biol. 88, 851 (2010).
54. M.-P. Caby, D. Lankar, C. Vincendeau-Scherrer, G. Raposo, and C. Bonnerot, Exosomal-like vesicles are present in human blood plasma. Int. Immunol. 17, 879 (2005).
55. D.-S. Choi, J.-M. Lee, G. W. Park, H.-W. Lim, J. Y. Bang, Y.-K. Kim, K.-H. Kwon, H. J. Kwon, K. P. Kim, and Y. S. Gho, Proteomic analysis of microvesicles derived from human colorectal cancer cells. J. Proteome. Res. 6, 4646 (2007).
56. C. Geminard, F. Nault, R. M. Johnstone, and M. Vidal, Characteristics of the interaction between Hsc70 and the transferrin receptor in exosomes released during reticulocyte maturation. J. Biol. Chem. 276, 9910 (2001).
57. C. Looze, D. Yui, L. Leung, M. Ingham, M. Kaler, X. Yao, W. W. Wu, R.-F.Shen, M. P. Daniels, and S. J. Levine, Proteomic profiling of human plasma exosomes identifies PPARgamma as an exosomeassociated protein. Biochem. Biophys. Res. Commun. 378, 433 (2009).
58. A. Savina, M. Vidal, and M. I. Colombo, The exosome pathway in K562 cells is regulated by Rab11. J. Cell Sci. 115, 2505 (2002).
59. C. Subra, D. Grand, K. Laulagnier, A. Stella, G. Lambeau, M. Paillasse, P. De Medina, B. Monsarrat, B. Perret, S. Silvente-Poirot, M. Poirot, and M. Record, Exosomes account for vesiclemediated transcellular transport of activatable phospholipases and prostaglandins. J. Lipid. Res. 51, 2105 (2010).
60. F. H. Jansen, J. Krijgsveld, A. van Rijswijk, G.-J. van den Bemd, M. S. van den Berg, W. M. van Weerden, R. Willemsen, L. J. Dekker, T. M. Luider, and G. Jenster, Exosomal secretion of cytoplasmic prostate cancer xenograft-derived proteins. Mol. Cell Proteomics 8, 1192 (2009).
61. H. W. King, M. Z. Michael, and J. M. Gleadle, Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 12, 421 (2012).
62. L. Ramachandra, Y. Qu, Y. Wang, C. J. Lewis, B. A. Cobb, K. Takatsu, W. H. Boom, G. R. Dubyak, and C. V. Harding, Mycobacterium tuberculosis synergizes with ATP to induce release of microvesicles and exosomes containing major histocompatibility complex class II molecules capable of antigen presentation. Infect. Immun. 78, 5116 (2010).
63. C. Salomon, J. Ryan, L. Sobrevia, M. Kobayashi, K. Ashman, M. Mitchell, and G. E. Rice, Exosomal signaling during hypoxia mediates microvascular endothelial cell migration and vasculogenesis. PLoS One 8, e68451 (2013).
64. A. Shibuya and N. Ikewaki, High serum glyceraldehyde-3-phosphate dehydrogenase levels in patients with liver cirrhosis. Hepatol Res. 22, 174 (2002).
65. P. E. Glaser, X. Han, and R. W. Gross, Tubulin is the endogenous inhibitor of the glyceraldehyde 3-phosphate dehydrogenase isoform that catalyzes membrane fusion: Implications for the coordinated regulation of glycolysis and membrane fusion. Proc. Natl. Acad. Sci. USA 99, 14104 (2002).