Skip to main content

Advertisement

SpringerLink
Log in

A Peptide Targeting Inflammatory CNS Lesions in the EAE Rat Model of Multiple Sclerosis

  • ORIGINAL ARTICLE
  • Published:
Inflammation Aims and scope Submit manuscript

Abstract

Multiple sclerosis is characterized by inflammatory lesions dispersed throughout the central nervous system (CNS) leading to severe neurological handicap. Demyelination, axonal damage, and blood brain barrier alterations are hallmarks of this pathology, whose precise processes are not fully understood. In the experimental autoimmune encephalomyelitis (EAE) rat model that mimics many features of human multiple sclerosis, the phage display strategy was applied to select peptide ligands targeting inflammatory sites in CNS. Due to the large diversity of sequences after phage display selection, a bioinformatics procedure called “PepTeam” designed to identify peptides mimicking naturally occurring proteins was used, with the goal to predict peptides that were not background noise. We identified a circular peptide CLSTASNSC called “Ph48” as an efficient binder of inflammatory regions of EAE CNS sections including small inflammatory lesions of both white and gray matter. Tested on human brain endothelial cells hCMEC/D3, Ph48 was able to bind efficiently when these cells were activated with IL1β to mimic inflammatory conditions. The peptide is therefore a candidate for further analyses of the molecular alterations in inflammatory lesions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Lubetzki, C., and B. Stankoff. 2014. Demyelination in multiple sclerosis. Handbook of Clinical Neurology 122: 89–99. https://doi.org/10.1016/B978-0-444-52001-2.00004-2.

    Article  PubMed  Google Scholar 

  2. Noseworthy, J.H., C. Lucchinetti, M. Rodriguez, and B.G. Weinshenker. 2000. Multiple sclerosis. The New England Journal of Medicine 343: 938–952. https://doi.org/10.1056/NEJM200009283431307.

    Article  PubMed  CAS  Google Scholar 

  3. Karlik, S.J., W.A. Roscoe, C. Patinote, and C. Contino-Pepin. 2012. Targeting vascular changes in lesions in multiple sclerosis and experimental autoimmune encephalomyelitis. Central Nervous System Agents in Medicinal Chemistry 12: 7–14.

    Article  PubMed  CAS  Google Scholar 

  4. Solomon, A.J., R. Watts, B.E. Dewey, and D.S. Reich. 2017. MRI evaluation of thalamic volume differentiates MS from common mimics. Neurology(R) Neuroimmunology & Neuroinflammation 4: e387. https://doi.org/10.1212/NXI.0000000000000387.

    Article  Google Scholar 

  5. Azevedo, C.J., E. Overton, S. Khadka, J. Buckley, S. Liu, M. Sampat, O. Kantarci, et al. 2015. Early CNS neurodegeneration in radiologically isolated syndrome. Neurology(R) Neuroimmunology & Neuroinflammation 2: e102. https://doi.org/10.1212/NXI.0000000000000102.

    Article  Google Scholar 

  6. Barkhof, F., P.A. Calabresi, D.H. Miller, and S.C. Reingold. 2009. Imaging outcomes for neuroprotection and repair in multiple sclerosis trials. Nature Reviews. Neurology 5: 256–266. https://doi.org/10.1038/nrneurol.2009.41.

    Article  PubMed  Google Scholar 

  7. Filippi, M., A. Charil, M. Rovaris, M. Absinta, and M. Assunta Rocca. 2014. Insights from magnetic resonance imaging. Handbook of Clinical Neurology 122: 115–149. https://doi.org/10.1016/B978-0-444-52001-2.00006-6.

    Article  PubMed  Google Scholar 

  8. Stoll, G., and M. Bendszus. 2009. Imaging of inflammation in the peripheral and central nervous system by magnetic resonance imaging. Neuroscience 158: 1151–1160. https://doi.org/10.1016/j.neuroscience.2008.06.045.

    Article  PubMed  CAS  Google Scholar 

  9. Tourdias, T., S. Roggerone, M. Filippi, M. Kanagaki, M. Rovaris, D.H. Miller, K.G. Petry, et al. 2012. Assessment of disease activity in multiple sclerosis phenotypes with combined gadolinium- and superparamagnetic iron oxide-enhanced MR imaging. Radiology 264: 225–233. https://doi.org/10.1148/radiol.12111416.

    Article  PubMed  Google Scholar 

  10. Boven, L.A., M. Van Meurs, M. Van Zwam, A. Wierenga-Wolf, R.Q. Hintzen, R.G. Boot, J.M. Aerts, S. Amor, E.E. Nieuwenhuis, and J.D. Laman. 2006. Myelin-laden macrophages are anti-inflammatory, consistent with foam cells in multiple sclerosis. Brain: A Journal of Neurology 129: 517–526. https://doi.org/10.1093/brain/awh707.

    Article  Google Scholar 

  11. Broholm, H., B. Andersen, B. Wanscher, J.L. Frederiksen, I. Rubin, B. Pakkenberg, H.B.W. Larsson, and M. Lauritzen. 2004. Nitric oxide synthase expression and enzymatic activity in multiple sclerosis. Acta Neurologica Scandinavica 109: 261–269.

    Article  PubMed  CAS  Google Scholar 

  12. Lucchinetti, C.F., R.H. Gavrilova, I. Metz, J.E. Parisi, B.W. Scheithauer, S. Weigand, K. Thomsen, et al. 2008. Clinical and radiographic spectrum of pathologically confirmed tumefactive multiple sclerosis. Brain: A Journal of Neurology 131: 1759–1775. https://doi.org/10.1093/brain/awn098.

    Article  CAS  Google Scholar 

  13. Trebst, C., F. König, R. Ransohoff, W. Brück, and M. Stangel. 2008. CCR5 expression on macrophages/microglia is associated with early remyelination in multiple sclerosis lesions. Multiple Sclerosis (Houndmills, Basingstoke, England) 14: 728–733. https://doi.org/10.1177/1352458508089359.

    Article  CAS  Google Scholar 

  14. Berger, C., P. Hiestand, D. Kindler-Baumann, M. Rudin, and M. Rausch. 2006. Analysis of lesion development during acute inflammation and remission in a rat model of experimental autoimmune encephalomyelitis by visualization of macrophage infiltration, demyelination and blood-brain barrier damage. NMR in Biomedicine 19: 101–107. https://doi.org/10.1002/nbm.1007.

    Article  PubMed  Google Scholar 

  15. Tommasin, S., C. Giannì, L. De Giglio, and P. Pantano. 2017. Neuroimaging techniques to assess inflammation in multiple sclerosis. Neuroscience. https://doi.org/10.1016/j.neuroscience.2017.07.055.

  16. Dousset, V., B. Brochet, M.S.A. Deloire, L. Lagoarde, B. Barroso, J.-M. Caille, and K.G. Petry. 2006. MR imaging of relapsing multiple sclerosis patients using ultra-small-particle iron oxide and compared with gadolinium. AJNR. American Journal of Neuroradiology 27: 1000–1005.

    PubMed  CAS  Google Scholar 

  17. Vellinga, M.M., R.D. Oude Engberink, A. Seewann, P.J.W. Pouwels, M.P. Wattjes, S.M.A. van der Pol, C. Pering, et al. 2008. Pluriformity of inflammation in multiple sclerosis shown by ultra-small iron oxide particle enhancement. Brain: A Journal of Neurology 131: 800–807. https://doi.org/10.1093/brain/awn009.

    Article  Google Scholar 

  18. Engelhardt, B. 2008. Immune cell entry into the central nervous system: Involvement of adhesion molecules and chemokines. Journal of the Neurological Sciences 274: 23–26. https://doi.org/10.1016/j.jns.2008.05.019.

    Article  PubMed  CAS  Google Scholar 

  19. Absinta, M., G. Nair, P. Sati, I.C.M. Cortese, M. Filippi, and D.S. Reich. 2015. Direct MRI detection of impending plaque development in multiple sclerosis. Neurology(R) Neuroimmunology & Neuroinflammation 2: e145. https://doi.org/10.1212/NXI.0000000000000145.

    Article  Google Scholar 

  20. Cramer, S.P., H. Simonsen, J.L. Frederiksen, E. Rostrup, and H.B.W. Larsson. 2014. Abnormal blood-brain barrier permeability in normal appearing white matter in multiple sclerosis investigated by MRI. NeuroImage. Clinical 4: 182–189. https://doi.org/10.1016/j.nicl.2013.12.001.

    Article  PubMed  CAS  Google Scholar 

  21. Kidd, D., F. Barkhof, R. McConnell, P.R. Algra, I.V. Allen, and T. Revesz. 1999. Cortical lesions in multiple sclerosis. Brain: A Journal of Neurology 122 (Pt 1): 17–26.

    Article  Google Scholar 

  22. Parisi, L., M.A. Rocca, F. Mattioli, G.C. Riccitelli, R. Capra, C. Stampatori, F. Bellomi, and M. Filippi. 2014. Patterns of regional gray matter and white matter atrophy in cortical multiple sclerosis. Journal of Neurology 261: 1715–1725. https://doi.org/10.1007/s00415-014-7409-5.

    Article  PubMed  Google Scholar 

  23. Smith, G.P. 1985. Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science (New York, N.Y.) 228: 1315–1317.

    Article  CAS  Google Scholar 

  24. Deutscher, S.L. 2010. Phage display in molecular imaging and diagnosis of cancer. Chemical Reviews 110: 3196–3211. https://doi.org/10.1021/cr900317f.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Rakonjac, J., N.J. Bennett, J. Spagnuolo, D. Gagic, and M. Russel. 2011. Filamentous bacteriophage: biology, phage display and nanotechnology applications. Current Issues in Molecular Biology 13: 51–76.

    PubMed  CAS  Google Scholar 

  26. Arap, W., M.G. Kolonin, M. Trepel, J. Lahdenranta, M. Cardó-Vila, R.J. Giordano, P.J. Mintz, et al. 2002. Steps toward mapping the human vasculature by phage display. Nature Medicine 8: 121–127. https://doi.org/10.1038/nm0202-121.

    Article  PubMed  CAS  Google Scholar 

  27. Pasqualini, R., and E. Ruoslahti. 1996. Organ targeting in vivo using phage display peptide libraries. Nature 380: 364–366. https://doi.org/10.1038/380364a0.

    Article  PubMed  CAS  Google Scholar 

  28. van Rooy, I., S. Cakir-Tascioglu, P.-O. Couraud, I.A. Romero, B. Weksler, G. Storm, W.E. Hennink, R.M. Schiffelers, and E. Mastrobattista. 2010. Identification of peptide ligands for targeting to the blood-brain barrier. Pharmaceutical Research 27: 673–682. https://doi.org/10.1007/s11095-010-0053-6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Weksler, B.B., E.A. Subileau, N. Perrière, P. Charneau, K. Holloway, M. Leveque, H. Tricoire-Leignel, et al. 2005. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 19: 1872–1874. https://doi.org/10.1096/fj.04-3458fje.

    Article  CAS  Google Scholar 

  30. Ransohoff, Richard M. 2012. Animal models of multiple sclerosis: the good, the bad and the bottom line. Nature Neuroscience 15: 1074–1077. https://doi.org/10.1038/nn.3168.

    Article  PubMed  CAS  Google Scholar 

  31. Boullerne, A.I., J.J. Rodriguez, T. Touil, B. Brochet, S. Schmidt, N.D. Abrous, M. Le Moal, et al. 2002. Anti-S-nitrosocysteine antibodies are a predictive marker for demyelination in experimental autoimmune encephalomyelitis: Implications for multiple sclerosis. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 22: 123–132.

    Article  CAS  Google Scholar 

  32. Coisne, C., L. Dehouck, C. Faveeuw, Y. Delplace, F. Miller, C. Landry, C. Morissette, et al. 2005. Mouse syngenic in vitro blood-brain barrier model: A new tool to examine inflammatory events in cerebral endothelium. Laboratory Investigation; a Journal of Technical Methods and Pathology 85: 734–746. https://doi.org/10.1038/labinvest.3700281.

    Article  PubMed  CAS  Google Scholar 

  33. Kolb, G., and C. Boiziau. 2005. Selection by phage display of peptides targeting the HIV-1 TAR element. RNA Biology 2: 28–33.

    Article  PubMed  CAS  Google Scholar 

  34. Weksler, B., I.A. Romero, and P.-O. Couraud. 2013. The hCMEC/D3 cell line as a model of the human blood brain barrier. Fluids and barriers of the CNS 10: 16. https://doi.org/10.1186/2045-8118-10-16.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Liebner, S., M. Corada, T. Bangsow, J. Babbage, A. Taddei, C.J. Czupalla, M. Reis, et al. 2008. Wnt/beta-catenin signaling controls development of the blood-brain barrier. The Journal of Cell Biology 183: 409–417. https://doi.org/10.1083/jcb.200806024.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Ramirez, S.H., S. Fan, M. Zhang, A. Papugani, N. Reichenbach, H. Dykstra, A.J. Mercer, R.F. Tuma, and Y. Persidsky. 2010. Inhibition of glycogen synthase kinase 3beta (GSK3beta) decreases inflammatory responses in brain endothelial cells. The American Journal of Pathology 176: 881–892. https://doi.org/10.2353/ajpath.2010.090671.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Hillyer, P., E. Mordelet, G. Flynn, and D. Male. 2003. Chemokines, chemokine receptors and adhesion molecules on different human endothelia: discriminating the tissue-specific functions that affect leucocyte migration. Clinical and Experimental Immunology 134: 431–441.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Vargas-Sanchez, K., A. Vekris, and K.G. Petry. 2016. DNA subtraction of in vivo selected phage repertoires for efficient peptide pathology biomarker identification in neuroinflammation multiple sclerosis model. Biomarker Insights 11: 19–29. https://doi.org/10.4137/BMI.S32188.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Kolonin, M.G., J. Sun, K.-A. Do, C.I. Vidal, Y. Ji, K.A. Baggerly, R. Pasqualini, and W. Arap. 2006. Synchronous selection of homing peptides for multiple tissues by in vivo phage display. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 20: 979–981. https://doi.org/10.1096/fj.05-5186fje.

    Article  CAS  Google Scholar 

  40. Liang, X., H. Qin, L. Bo, D. McBride, H. Bian, P. Spagnoli, C. Di, J. Tang, and J.H. Zhang. 2014. Follistatin-like 1 attenuates apoptosis via disco-interacting protein 2 homolog A/Akt pathway after middle cerebral artery occlusion in rats. Stroke 45: 3048–3054. https://doi.org/10.1161/STROKEAHA.114.006092.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Ouchi, N., Y. Asaumi, K. Ohashi, A. Higuchi, S. Sono-Romanelli, Y. Oshima, and K. Walsh. 2010. DIP2A functions as a FSTL1 receptor. The Journal of Biological Chemistry 285: 7127–7134. https://doi.org/10.1074/jbc.M109.069468.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Zhang, L., H.A. Mabwi, N.J. Palange, R. Jia, J. Ma, F.B. Bah, R.K. Sah, et al. 2015. Expression patterns and potential biological roles of Dip2a. PLoS One 10: e0143284. https://doi.org/10.1371/journal.pone.0143284.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Jiao, J., M. Gao, H. Zhang, N. Wang, Z. Xiao, K. Liu, M. Yang, K. Wang, and X. Xiao. 2014. Identification of potential biomarkers by serum proteomics analysis in rats with sepsis. Shock (Augusta, Ga.) 42: 75–81. https://doi.org/10.1097/SHK.0000000000000173.

    Article  CAS  Google Scholar 

  44. Matthews, K.W., S.L. Mueller-Ortiz, and R.A. Wetsel. 2004. Carboxypeptidase N: A pleiotropic regulator of inflammation. Molecular Immunology 40: 785–793.

    Article  PubMed  CAS  Google Scholar 

  45. Cattaneo, E., C. Zuccato, and M. Tartari. 2005. Normal huntingtin function: an alternative approach to Huntington’s disease. Nature Reviews. Neuroscience 6: 919–930. https://doi.org/10.1038/nrn1806.

    Article  PubMed  CAS  Google Scholar 

  46. Schultz, G.S., and A. Wysocki. 2009. Interactions between extracellular matrix and growth factors in wound healing. Wound Repair and Regeneration: Official Publication of the Wound Healing Society [and] the European Tissue Repair Society 17: 153–162. https://doi.org/10.1111/j.1524-475X.2009.00466.x.

    Article  Google Scholar 

  47. Duffy, S.S., J.G. Lees, and G. Moalem-Taylor. 2014. The contribution of immune and glial cell types in experimental autoimmune encephalomyelitis and multiple sclerosis. Multiple Sclerosis International 2014: 285245. https://doi.org/10.1155/2014/285245.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Engelhardt, B., and S. Liebner. 2014. Novel insights into the development and maintenance of the blood-brain barrier. Cell and Tissue Research 355: 687–699. https://doi.org/10.1007/s00441-014-1811-2.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Lengfeld, J., T. Cutforth, and D. Agalliu. 2014. The role of angiogenesis in the pathology of multiple sclerosis. Vascular Cell 6: 23. https://doi.org/10.1186/s13221-014-0023-6.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Pinheiro Lopez, M.A., G. Kooij, M.R. Mizee, A. Kamermans, G. Enzmann, R. Lyck, M. Schwaninger, B. Engelhardt, and H.E. de Vries. 2016. Immune cell trafficking across the barriers of the central nervous system in multiple sclerosis and stroke. Biochimica et Biophysica Acta 1862: 461–471. https://doi.org/10.1016/j.bbadis.2015.10.018.

    Article  CAS  Google Scholar 

  51. Luissint, A.-C., C. Artus, F. Glacial, K. Ganeshamoorthy, and P.-O. Couraud. 2012. Tight junctions at the blood brain barrier: physiological architecture and disease-associated dysregulation. Fluids and barriers of the CNS 9: 23. https://doi.org/10.1186/2045-8118-9-23.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Gauberti, M., A. Montagne, A. Quenault, and D. Vivien. 2014. Molecular magnetic resonance imaging of brain-immune interactions. Frontiers in Cellular Neuroscience 8: 389. https://doi.org/10.3389/fncel.2014.00389.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Li, J., Q. Zhang, Z. Pang, Y. Wang, Q. Liu, L. Guo, and X. Jiang. 2012. Identification of peptide sequences that target to the brain using in vivo phage display. Amino Acids 42: 2373–2381. https://doi.org/10.1007/s00726-011-0979-y.

    Article  PubMed  CAS  Google Scholar 

  54. Smith, M.W., G. Al-Jayyoussi, and M. Gumbleton. 2012. Peptide sequences mediating tropism to intact blood-brain barrier: an in vivo biodistribution study using phage display. Peptides 38: 172–180. https://doi.org/10.1016/j.peptides.2012.06.019.

    Article  PubMed  CAS  Google Scholar 

  55. Tani, H., J.K. Osbourn, E.H. Walker, R.A. Rush, and I.A. Ferguson. 2013. A novel in vivo method for isolating antibodies from a phage display library by neuronal retrograde transport selectively yields antibodies against p75(NTR.). MAbs 5: 471–478. https://doi.org/10.4161/mabs.24112.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Wan, X.M., Y.P. Chen, W.R. Xu, W.J. Yang, and L.P. Wen. 2009. Identification of nose-to-brain homing peptide through phage display. Peptides 30: 343–350. https://doi.org/10.1016/j.peptides.2008.09.026.

    Article  PubMed  CAS  Google Scholar 

  57. Jones, A.R., C.C. Stutz, Y. Zhou, J.D. Marks, and E.V. Shusta. 2014. Identifying blood-brain-barrier selective single-chain antibody fragments. Biotechnology Journal 9: 664–674. https://doi.org/10.1002/biot.201300550.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Yang, M, C. Liu, M. Niu, Y. Hu, M. Guo, J. Zhang, Y. Luo, et al. 2014. Phage-display library biopanning and bioinformatic analysis yielded a high-affinity peptide to inflamed vascular endothelium both in vitro and in vivo. Journal of Controlled Release: Official Journal of the Controlled Release Society 174: 72–80. https://doi.org/10.1016/j.jconrel.2013.11.009.

    Article  CAS  Google Scholar 

  59. Reynolds, F., N. Panneer, C.M. Tutino, W. Michael, W.R. Skrabal, C. Moskaluk, and K.A. Kelly. 2011. A functional proteomic method for biomarker discovery. PLoS One 6: e22471. https://doi.org/10.1371/journal.pone.0022471.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Laderach, D.J., L. Gentilini, F.M. Jaworski, and D. Compagno. 2013. Galectins as new prognostic markers and potential therapeutic targets for advanced prostate cancers. Prostate Cancer 519436. https://doi.org/10.1155/2013/519436.

  61. Mendez-Huergo, S.P., S.M. Maller, M.F. Farez, K. Mariño, J. Correale, and G.A. Rabinovich. 2014. Integration of lectin-glycan recognition systems and immune cell networks in CNS inflammation. Cytokine & Growth Factor Reviews 25: 247–255. https://doi.org/10.1016/j.cytogfr.2014.02.003.

    Article  CAS  Google Scholar 

  62. Sato, S., C. St-Pierre, P. Bhaumik, and J. Nieminen. 2009. Galectins in innate immunity: dual functions of host soluble beta-galactoside-binding lectins as damage-associated molecular patterns (DAMPs) and as receptors for pathogen-associated molecular patterns (PAMPs). Immunological Reviews 230: 172–187. https://doi.org/10.1111/j.1600-065X.2009.00790.x.

    Article  PubMed  CAS  Google Scholar 

  63. Stancic, M., J. van Horssen, V.L. Thijssen, H.-J. Gabius, P. van der Valk, D. Hoekstra, and W. Baron. 2011. Increased expression of distinct galectins in multiple sclerosis lesions. Neuropathology and Applied Neurobiology 37: 654–671. https://doi.org/10.1111/j.1365-2990.2011.01184.x.

    Article  PubMed  CAS  Google Scholar 

  64. Ilarregui, J.M., D.O. Croci, G.A. Bianco, M.A. Toscano, M. Salatino, M.E. Vermeulen, J.R. Geffner, and G.A. Rabinovich. 2009. Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nature Immunology 10: 981–991. https://doi.org/10.1038/ni.1772.

    Article  PubMed  CAS  Google Scholar 

  65. McAteer, M.A., N.R. Sibson, C. von Zur Muhlen, J.E. Schneider, A.S. Lowe, N. Warrick, K.M. Channon, D.C. Anthony, and R.P. Choudhury. 2007. In vivo magnetic resonance imaging of acute brain inflammation using microparticles of iron oxide. Nature Medicine 13: 1253–1258. https://doi.org/10.1038/nm1631.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

AKNOWLEDGEMENTS

This work was supported by grants from ANR-TecSan, INSERM ANR preciput, ARSEP and the Conseil Régional d’Aquitaine (France). KVS received a doctoral fellowship from the European Network Council ENC-Network. We also thank Pr P.O. Couraud (Institut Cochin, Paris, France) for the hCMEC/D3 cell line; Pr Marc Bonneu (CBMN Bordeaux, France) for the proteomic analysis; and our colleagues M.S. Deloire, N. Dubourdieu-Cassagno, F. Ottones, and A. Vekris for the technical assistance and helpful discussions.

Author information

Author notes

  1. Claudine Boiziau

    Present address: INSERM, UMR 1026, BioTis, F-33 076, Bordeaux, France

  2. Karina Vargas-Sanchez

    Present address: Biomedical Sciences Research Group, GRINCIBIO, School of Medicine, Universidad Antonio Nariño, Bogotà, Colombia

  3. Klaus G. Petry

    Present address: INSERM, UMR1029, F-33076, Bordeaux, France

Authors and Affiliations

  1. INSERM, UMR 1049, F-33076, Bordeaux, France

    Claudine Boiziau, Elodie Mordelet, Justine Aussudre, Karina Vargas-Sanchez & Klaus G. Petry

  2. Univ. Bordeaux, Neuroinflammation Imaging and Therapy of Multiple Sclerosis, F-33076, Bordeaux, France

    Claudine Boiziau, Elodie Mordelet, Justine Aussudre, Karina Vargas-Sanchez & Klaus G. Petry

  3. Univ. Bordeaux, CBiB, F-33076, Bordeaux, France

    Macha Nikolski

  4. CNRS, LaBRI UMR 5800, F-33400, Talence, France

    Macha Nikolski

Authors
  1. Claudine Boiziau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Macha Nikolski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elodie Mordelet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Justine Aussudre
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Karina Vargas-Sanchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Klaus G. Petry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudine Boiziau.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (animal experimentation permission, France 33/00055).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boiziau, C., Nikolski, M., Mordelet, E. et al. A Peptide Targeting Inflammatory CNS Lesions in the EAE Rat Model of Multiple Sclerosis. Inflammation 41, 932–947 (2018). https://doi.org/10.1007/s10753-018-0748-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10753-018-0748-0

Key Words

Search

Navigation