Design and Screening of a Glial Cell-Specific, Cell Penetrating Peptide for Therapeutic Applications in Multiple Sclerosis

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Heffernan, Corey ^a   Sumer, Huseyin ^a   Guillemin, Gilles J ^b   Manuelpillai, Ursula ^a   Verma, Paul J ^a,c  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c SOUTH AUSTRALIAN RESEARCH AND DEVELOPMENT INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PENETRATING PEPTIDE; POLYHISTIDINE TAG; TD2 2 PEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; ASTROCYTE; BINDING AFFINITY; CELL MIGRATION; CONCEPTUAL FRAMEWORK; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG MECHANISM; EXPRESSION VECTOR; GLIA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MULTIPLE SCLEROSIS; NERVE CELL; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PROGENY; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN TRANSPORT; SKIN FIBROBLAST;

AMINO ACID SEQUENCE; ASTROCYTES; BIOLOGICAL TRANSPORT; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL-PENETRATING PEPTIDES; DERMIS; DRUG DESIGN; ESCHERICHIA COLI; FIBROBLASTS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; MULTIPLE SCLEROSIS; NEURAL STEM CELLS; OLIGODENDROGLIA; ORGAN SPECIFICITY; RECOMBINANT FUSION PROTEINS; TIME-LAPSE IMAGING;

EID: 84866705894     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045501     Document Type: Article

References (44)

1. Milward E, Kim KJ, Szklarczyk A, Nguyen T, Melli G, et al. (2008) Cleavage of myelin associated glycoprotein by matrix metalloproteinases. J Neuroimmunol 193(1-2): 140-8.
2. Axtell RC, de Jong BA, Boniface K, van der Voort LF, Bhat R, et al. (2010) T helper type 1 and 17 cells determine efficacy of interferon-B in multiple sclerosis and experimental encephalomyelitis. Nat Med 16(4): 406-413.
3. Johansson HJ, Andaloussi SE, Langel U, (2011) Mimicry of protein function with cell-penetrating peptides. Methods Mol Biol 683: 233-4.
4. Derossi D, Joliot AH, Chassaing G, Prochiantz A, (1994) The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 269: 10444-10450.
5. Derossi D, Calvet S, Trembleau A, Brunissen A, Chassaing G, et al. (1996) Cell internalization of the third helix of the antennapedia homeodomain is receptor-independent. J Biol Chem 271: 18188-18193.
6. Frankel AD, Pabo CO, (1988) Cellular uptake of the Tat protein from human immunodeficiency virus. Cell 55: 1189-1193.
7. Green M, Loewenstein PM, (1988) Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 55(6): 1179-88.
8. Rusnati M, Tulipano G, Spillmann D, Tanghetti E, Oreste P, et al. (1999) Multiple interactions of HIV-1 Tat protein with size-defined heparin oligosaccharides. J Biol Chem 274(40): 8198-28205.
9. Tyagi M, Rusnati M, Presta M, Giacca M, (2001) Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 276(5): 3254-3261.
10. Fittipaldi A, Ferrari A, Zoppé M, Arcangeli C, Pellegrini V, et al. (2003) Cell membrane lipid rafts mediate caveolar endocytosis of HIV Tat fusion proteins. J Biol Chem 278(36): 34141-34149.
11. Efthymiadis A, Briggs LJ, Jans DA, (1998) The HIV-1 Tat nuclear localization sequence confers novel nuclear import properties. J Biol Chem 273(3): 1623-1628.
12. Heffernan C, Sumer H, Malaver-Ortega LF, Verma PJ (2012) Temporal requirements of cMyc protein for reprogramming mouse fibroblasts. Stem Cells Int. In press.
13. Kim D, Kim CH, Moon JI, Chung YG, Chang MY, et al. (2009) Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4: 472-476.
14. Zhou H, Wu S, Joo JY, Zhu S, Han DW, et al. (2009) Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4(5): 381-384.
15. Chian RJ, Li J, Ay I, Celia SA, Kashi BB, et al. (2009) IGF-1:tetanus toxin fragment C fusion protein improves delivery of IGF-1 to spinal cord but fails to prolong survival of ALS mice. Brain Res 1287: 1-19.
16. Benn SC, Ay I, Bastia E, Chian RJ, Celia SA, et al. (2005) Tetanus toxin fragment C fusion facilitates protein delivery to CNS neurons from cerebrospinal fluid in mice. J Neurochem 95(4): 1118-31.
17. Larsen KE, Benn SC, Ay I, Chian RJ, Celia SA, et al. (2006) A glial cell line-derived neurotrophic factor (GDNF):tetanus toxin fragment C protein conjugate improves delivery of GDNF to spinal cord motor neurons in mice. Brain Res 1120(1): 1-12.
18. Ravichandran V, Major EO, (2006) Viral proteomics: a promising approach for understanding JC virus tropism. Proteomics 6(20): 5628-36.
19. Kunz S, Sevilla N, McGavern DB, Campbell KP, Oldstone MB, (2001) Molecular analysis of the interaction of LCMV with its cellular receptor [alpha]-dystroglycan. J Cell Biol 155(2): 301-10.
20. Sullivan BM, Emonet SF, Welch MJ, Lee AM, Campbell KP, et al. (2011) Point mutation in the glycoprotein of lymphocytic choriomeningitis virus is necessary for receptor binding, dendritic cell infection, and long-term persistence. Proc Natl Acad Sci USA 108(7): 2969-74.
21. Song JH, Bellail A, Tse MC, Yong VW, Hao C, (2006) Human astrocytes are resistant to Fas ligand and tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis. J Neurosci 26(12): 3299-308.
22. Back SA, Tuohy TM, Chen H, Wallingford N, Craig A, et al. (2005) Hyaluron accumulates in demyelinated lesions and inhibits oligodendrocytes progenitor maturation. Nat Med 11(9): 966-972.
23. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, et al. (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109(1): 75-86.
24. Borrow P, Oldstone MB, (1992) Characterization of lymphocytic choriomeningitis virus-binding protein(s): a candidate cellular receptor for the virus. J Virol 66(12): 7270-81.
25. Yamada H, Denzer AJ, Hori H, Tanaka T, Anderson LV, et al. (1996) Dystroglycan is a dual receptor for agrin and laminin-2 in Schwann cell membrane. J Biol Chem 271(38): 23418-23.
26. Gesemann M, Brancaccio A, Schumacher B, Ruegg MA, (1998) Agrin is a high-affinity binding protein of dystroglycan in non-muscle tissue. J Biol Chem 273(1): 600-5.
27. Rambukkana A, Kunz S, Min J, Campbell KP, Oldstone MB, (2003) Targeting Schwann cells by nonlytic arenaviral infection selectively inhibits myelination. Proc Natl Acad Sci USA 100(26): 16071-6.
28. Lim CK, Smythe GA, Stocker R, Brew BJ, Guillemin GJ, (2007) Characterization of the kynurenine pathway in human oligodendrocytes. International Congress Series 1304: 213-217.
29. McLaurin J, Trudel GC, Shaw IT, Antel JP, Cashman NR, (1995) A human glial hybrid cell line differentially expressing genes subserving oligodendrocyte and astrocyte phenotype. J Neurobiol 26: 283-293.
30. Buntinx M, Vanderlocht J, Hellings N, Vandenabeele F, Lambrichts I, et al. (2003) Characterization of three human oligodendroglial cell lines as a model to study oligodendrocyte injury: morphology and oligodendrocyte-specific gene expression. J Neurocytol 32(1): 25-38.
31. Pan C, Lu B, Chen H, Bishop CE, (2010) Reprogramming human fibroblasts using HIV-1 TAT recombinant proteins OCT4, SOX2, KLF4 and c-MYC. Mol Biol Rep 37(4): 2117-24.
32. Heffernan C, Whiley PA, Milionis A, Verma PJ, Holland MK, (2010) Lineage-specific expression of heterochromatin protein 1gamma in post-compaction, in vitro-produced bovine embryos. Reprod Fertil Dev 22(6): 1022-31.
33. Morita S, Kojima T, Kitamura T, (2000) Plat-E: an efficient and stable system for transient packaging of retrovirus. Gene Therapy 7: 1063-1066.
34. Sgambato A, Migaldi M, Montanari M, Camerini A, Brancaccio A, et al. (2003) Dystroglycan expression is frequently reduced in human breast and colon cancers and is associated with tumor progression. Am J Pathol 162(3): 849-60.
35. Sawant R, Torchilin V, (2010) Intracellular transduction using cell-penetrating peptides. Mol Biosyst 6(4): 628-40.
36. Maginnis MS, Atwood WJ, (2009) JC virus: an oncogenic virus in animals and humans? Semin Cancer Biol 19(4): 261-9.
37. Huang JK, Jarjour AA, Nait Oumesmar B, Kerninon C, Williams A, et al. (2011) Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat Neurosci 14(1): 45-53.
38. Ren Z, Wang Y, Tao D, Liebenson D, Liggett T, et al. (2011) Overexpression of the dominant-negative form of interferon regulatory factor 1 in oligodendrocytes protects against experimental autoimmune encephalomyelitis. J Neurosci 31(23): 8329-41.
39. McCandless EE, Budde M, Lees JR, Dorsey D, Lyng E, et al. (2009) IL-1R signaling within the central nervous system regulates CXCL12 expression at the blood-brain barrier and disease severity during experimental autoimmune encephalomyelitis. J Immunol. 183(1): 613-20.
40. Ichimura K, Pearson DM, Kocialkowski S, Bäcklund LM, Chan R, et al. (2009) IDH1 mutations are present in the majority of common adult gliomas but rare in primary glioblastomas. Neuro-Oncology 11: 341-347.
41. Aktaş Y, Yemisci M, Andrieux K, Gürsoy RN, Alonso MJ, et al. (2005) Development and brain delivery of chitosan-PEG nanoparticles functionalized with the monoclonal antibody OX26. Bioconjug Chem 16(6): 1503-11.
42. Stork R, Müller D, Kontermann RE, (2007) A novel tri-functional antibody fusion protein with improved pharmacokinetic properties generated by fusing a bispecific single-chain diabody with an albumin-binding domain from streptococcal protein G. Prot Eng Des Select. 20(11): 569-76.
43. Bowie JU, Sauer RT, (1989) Identification of C-terminal extensions that protect proteins from intracellular proteolysis. J Biol Chem 264(13): 7596-7602.
44. Goyal A, Batra JK, (2000) Inclusion of a furin-sensitive spacer enhances the cytotoxicity of ribotoxin retrictocin containing recombinant single-chain immunotoxins. Biochem J 345: 247-254.