Structure-Function Analysis of the Glioma Targeting NFL-TBS.40-63 Peptide Corresponding to the Tubulin-Binding Site on the Light Neurofilament Subunit

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Berges, Raphael ^a   Balzeau, Julien ^a   Takahashi, Masayuki ^a,b   Prevost, Chantal ^a,c   Eyer, Joel ^a  

^a ANGERS UNIVERSITY HOSPITAL   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c France   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ANTINEOPLASTIC AGENT; ASPARTIC ACID; LIGHT NEUROFILAMENT SUBUNIT TUBULIN BINDING SITE 40-63 PROTEIN; NEUROFILAMENT PROTEIN; PHOSPHOSERINE; SERINE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; BETA SHEET; CIRCULAR DICHROISM; CONTROLLED STUDY; DRUG ACTIVITY; DRUG CONFORMATION; DRUG PENETRATION; DRUG SELECTIVITY; DRUG STABILITY; DRUG TARGETING; GLIOMA CELL; HUMAN; HUMAN CELL; INTERNALIZATION; MICROTUBULE; MOLECULAR MODEL; PHOSPHORYLATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; REGULATORY MECHANISM; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

ALANINE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BINDING SITES; BRAIN NEOPLASMS; CELL LINE, TUMOR; CIRCULAR DICHROISM; ENDOCYTOSIS; GLIOMA; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTANT PROTEINS; NEUROFILAMENT PROTEINS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STABILITY; STRUCTURE-ACTIVITY RELATIONSHIP; TUBULIN;

EID: 84869017332     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049436     Document Type: Article

References (49)

1. Lee MK, Cleveland DW, (1996) Neuronal intermediate filaments. Annual Review of Neuroscience 19: 187-217.
2. Hirokawa N, (1982) Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method. The Journal of cell biology 94: 129-142.
3. Carden MJ, Trojanowski JQ, Schlaepfer WW, Lee VM, (1987) Two-stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns. The Journal of Neuroscience 7: 3489-3504.
4. Eyer J, Leterrier JF, (1988) Influence of the phosphorylation state of neurofilament proteins on the interactions between purified filaments in vitro. Biochemical journal 252: 655-660.
5. Eyer J, Peterson A, (1994) Neurofilament-deficient axons and perikaryal aggregates in viable transgenic mice expressing a neurofilament-beta-galactosidase fusion protein. Neuron 12: 389-405.
6. Zhu QZ, Couillard-Despres S, Julien JP, (1997) Delayed maturation of regenerating myelinated axons in mice lacking neurofilaments. Experimental Neurology 148: 299-316.
7. Ohara O, Gahara Y, Miyake T, Teraoka H, Kitamura T, (1993) Neurofilament deficiency in quail caused by nonsense mutation in neurofilament-L gene. Journal of Cell Biology 121: 387-395.
8. Dewaegh SM, Lee VMY, Brady ST, (1992) Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal-transport by myelinating Schwann-cells. Cell 68: 451-463.
9. Hisanaga S, Hirokawa N, (1990) Dephosphorylation-induced interactions of neurofilaments with microtubules. The Journal of Biological Chemistry 265: 21852-21858.
10. Hisanaga S, Kusubata M, Okumura E, Kishimoto T, (1991) Phosphorylation of neurofilament H subunit at the tail domain by Cdc2 kinase dissociates the association to microtubules. Journal of Biological Chemistry 266: 21798-21803.
11. Miyasaka H, Okabe S, Ishiguro K, Uchida T, Hirokawa N, (1993) Interaction of the tail domain of high-molecular-weight subunits of neurofilaments with the COOH-terminal region of tubulin and its regulation by Tau-protein kinase-II. Journal of Biological Chemistry 268: 22695-22702.
12. Hirokawa N, Hisanaga S, Shiomura Y, (1988) MAP2 is a component of crossbridges between microtubules and neurofilaments in the neuronal cytoskeleton: quick-freeze, deep-etch immunoelectron microscopy and reconstitution studies. The Journal of Neuroscience 8: 2769-2779.
13. Bocquet A, Berges R, Frank R, Robert P, Peterson AC, et al. (2009) Neurofilaments Bind Tubulin and Modulate Its Polymerization. Journal of Neuroscience 29: 11043-11054.
14. Berges R, Balzeau J, Peterson AC, Eyer J, (2012) A tubulin binding peptide targets glioma cells disrupting their microtubules, blocking migration, and inducing apoptosis. Molecular Therapy 20: 1367-1377.
15. Yates DM, Manser C, De Vos KJ, Shaw CE, McLoughlin DM, et al. (2009) Neurofilament subunit (NFL) head domain phosphorylation regulates axonal transport of neurofilaments. European Journal of Cell Biology 88: 193-202.
16. Chen J, Serizawa T, Komiyama M, (2011) Binding analysis of peptides that recognize preferentially cis-azobenzene groups of synthetic polymers. Journal of Peptide Science 17: 163-168.
17. Guerrini R, Salvadori S, Rizzi A, Regoli D, Calo G, (2010) Neurobiology, Pharmacology, and Medicinal Chemistry of Neuropeptide S and Its Receptor. Medicinal Research Reviews 30: 751-777.
18. Zorko M, Langel U, (2005) Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Advanced Drug Delivery Reviews 57: 529-545.
19. Foerg C, Merkle HP, (2008) On the biomedical promise of cell penetrating peptides: Limits versus prospects. Journal of Pharmaceutical Sciences 97: 144-162.
20. Futaki S, Suzuki T, Ohashi W, Yagami T, Tanaka S, et al. (2001) Arginine-rich peptides- An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. Journal of Biological Chemistry 276: 5836-5840.
21. Perrot R, Berges R, Bocquet A, Eyer J, (2008) Review of the multiple aspects of neurofilament functions, and their possible contribution to neurodegeneration. Molecular Neurobiology 38: 27-65.
22. Julien JP, Mushynski WE, (1982) Multiple phosphorylation sites in mammalian neurofilament polypeptides. The Journal of Biological Chemistry 257: 10467-10470.
23. Hisanaga S, Gonda Y, Inagaki M, Ikai A, Hirokawa N, (1990) Effects of phosphorylation of the neurofilament L protein on filamentous structures. Cell Regulation 1: 237-248.
24. Mukai H, Toshimori M, Shibata H, Kitagawa M, Shimakawa M, et al. (1996) PKN associates and phosphorylates the head-rod domain of neurofilament protein. Journal of Biological Chemistry 271: 9816-9822.
25. Sihag RK, Jaffe H, Nixon RA, Rong XH, (1999) Serine-23 is a major protein kinase A phosphorylation site on the amino-terminal head domain of the middle molecular mass subunit of neurofilament proteins. Journal of Neurochemistry 72: 491-499.
26. Sihag RK, Nixon RA, (1991) Identification of Ser-55 as a major protein kinase-A phosphorylation site on the 70-kDa subunit of neurofilaments- Early turnover during axonal-transport. Journal of Biological Chemistry 266: 18861-18867.
27. Cleverley KE, Betts JC, Blackstock WP, Gallo JM, Anderton BH, (1998) Identification of novel in vitro PKA phosphorylation sites on the low and middle molecular mass neurofilament subunits by mass spectrometry. Biochemistry 37: 3917-3930.
28. Giasson BI, Mushynski WE, (1998) Intermediate filament disassembly in cultured dorsal root ganglion neurons is associated with amino-terminal head domain phosphorylation of specific subunits. Journal of Neurochemistry 70: 1869-1875.
29. Hashimoto R, Nakamura Y, Komai S, Kashiwagi Y, Matsumoto N, et al. (2000) Phosphorylation of neurofilament-L during LTD. Neuroreport 11: 2739-2742.
30. Trimpin S, Mixon AE, Stapels MD, Kim MY, Spencer PS, et al. (2004) Identification of endogenous phosphorylation sites of bovine medium and low molecular weight neurofilament proteins by tandem mass spectrometry. Biochemistry 43: 2091-2105.
31. Johnson WC Jr, (1990) Protein secondary structure and circular dichroism: a practical guide. Proteins 7: 205-214.
32. Norden B, Rodger A, Dafforn T, (2010) Linear dichroism and circular dichroism: a textbook on polarized-light spectroscopy. Royal Society of Chemistry (ISBN: 978-1-84755-902-9).
33. Waterhous DV, Johnson WC, (1994) Importance of environment in determining secondary structure in proteins. Biochemistry 33: 2121-2128.
34. Oehlke J, Krause E, Wiesner B, Beyermann M, Bienert M, (1997) Extensive cellular-uptake into endothelial cells of an amphipathic beta-sheet forming peptide. Febs Letters 415: 196-199.
35. Bellet-Amalric E, Blaudez D, Desbat B, Graner F, Gauthier F, et al. (2000) Interaction of the third helix of Antennapedia homeodomain and a phospholipid monolayer, studied by ellipsometry and PM-IRRAS at the air-water interface. Biochimica Et Biophysica Acta-Biomembranes 1467: 131-143.
36. Yang JT, Wu CS, Martinez HM, (1986) Calculation of protein conformation from circular dichroism. Methods in enzymology 130: 208-269.
37. Reed J, Reed TA, (1997) A set of constructed type spectra for the practical estimation of peptide secondary structure from circular dichroism. Analytical Biochemistry 254: 36-40.
38. Venyaminov SY, Baikalov IA, Shen ZM, Wu CSC, Yang JT, (1993) Circular dichroic analysis of denatured proteins- inclusion of denatured proteins in the reference set. Analytical Biochemistry 214: 17-24.
39. Maupetit J, Derreumaux P, Tuffery P, (2009) PEP-FOLD: an online resource for de novo peptide structure prediction. Nucleic Acids Research 37: W498-W503.
40. Maupetit J, Derreumaux P, Tuffery P, (2010) A Fast Method for Large-Scale De Novo Peptide and Miniprotein Structure Prediction. Journal of Computational Chemistry 31: 726-738.
41. Maupetit J, Tuffery P, Derreumaux P, (2007) A coarse-grained protein force field for folding and structure prediction. Proteins 69: 394-408.
42. Duvignaud JB, Leclerc D, Gagne SM, (2010) Structure and dynamics changes induced by 2,2,2-trifluoro-ethanol (TFE) on the N-terminal half of hepatitis C virus core protein. Biochemistry and Cell Biology-Biochimie Et Biologie Cellulaire 88: 315-323.
43. Kawaguchi A, Suzuki T, Kimura T, Sakai N, Ayabe T, et al. (2010) Functional analysis of an alpha-helical antimicrobial peptide derived from a novel mouse defensin-like gene. Biochemical and Biophysical Research Communications 398: 778-784.
44. Steckbeck JD, Craigo JK, Barnes CO, Montelaro RC, (2011) Highly Conserved Structural Properties of the C-terminal Tail of HIV-1 gp41 Protein Despite Substantial Sequence Variation among Diverse Clades: Implications for Functions in Viral Replication. Journal of Biological Chemistry 286: 27156-27166.
45. Jones DT, (1999) Protein secondary structure prediction based on position-specific scoring matrices. Journal of Molecular Biology 292: 195-202.
46. Hess B, Kutzner C, van der Spoel D, Lindahl E, (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation 4: 435-447.
47. Kaminski GA, Friesner RA, Tirado-Rives J, Jorgensen WL, (2001) Evaluation and Reparametrization of the OPLS-AA Force Field for Proteins via Comparison with Accurate Quantum Chemical Calculations on Peptides. Journal of Physical Chemistry B 105: 6474-6487.
48. Essman U, Perela L, Berkowitz ML, Darden T, Lee H, et al. (1995) A smooth particle mesh Ewald method. Journal of Chemical Physics 103: 8577-8592.
49. Humphrey W, Dalke A, Schulten K, (1996) VMD: Visual molecular dynamics. Journal of Molecular Graphics & Modelling 14: 33-38.