Tuftsin-driven experimental autoimmune encephalomyelitis recovery requires neuropilin-1

GLIA

Volumn 64, Issue 6, 2016, Pages 923-936

  Nissen, Jillian C ^a   Tsirka, Stella E ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Anti inflammatory; EAE; Mice; Microglia; Treg

Indexed keywords

IMMUNOGLOBULIN G; NEUROPILIN 1; TUFTSIN; IMMUNOLOGIC FACTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL POLARITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; IMMUNOSURVEILLANCE; INTRACELLULAR SIGNALING; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; WHITE MATTER LESION; ANIMAL; DISEASE MODEL; GENETICS; MACROPHAGE ACTIVATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNOLOGIC FACTORS; MACROPHAGE ACTIVATION; MICE, TRANSGENIC; MICROGLIA; MULTIPLE SCLEROSIS; NEUROPILIN-1; T-LYMPHOCYTES; TUFTSIN;

EID: 84975741742     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22972     Document Type: Article

References (74)

1. Abram CL, Roberge GL, Hu Y, Lowell CA. 2014. Comparative analysis of the efficiency and specificity of myeloid-Cre deleting strains using ROSA-EYFP reporter mice. J Immunol Methods 408:89-100.
2. Almolda B, Gonzalez B, Castellano B. 2011. Antigen presentation in EAE: Role of microglia, macrophages and dendritic cells. Front Biosci 16:1157-1171.
3. Appel SH, Beers DR, Henkel JS. 2010. T cell-microglial dialogue in Parkinson's disease and amyotrophic lateral sclerosis: Are we listening? Trends Immunol 31:7-17.
4. Arno B, Grassivaro F, Rossi C, Bergamaschi A, Castiglioni V, Furlan R, Greter M, Favaro R, Comi G, Becher B, Martino G, Muzio L. 2014. Neural progenitor cells orchestrate microglia migration and positioning into the developing cortex. Nat Commun 5:5611.
5. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. 2002. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963-970.
6. Babcock GF, Amoscato AA, Nishioka K. 1983. Effect of tuftsin on the migration, chemotaxis, and differentiation of macrophages and granulocytes. Ann N Y Acad Sci 419:64-74.
7. Becher B, Bechmann I, Greter M. 2006. Antigen presentation in autoimmunity and CNS inflammation: How T lymphocytes recognize the brain. J Mol Med 84:532-543.
8. Benveniste EN. 1997. Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis. J Mol Med (Berl) 75:165-173.
9. Bernard CC, Johns TG, Slavin A, Ichikawa M, Ewing C, Liu J, Bettadapura J. 1997. Myelin oligodendrocyte glycoprotein: A novel candidate autoantigen in multiple sclerosis. J Mol Med 75:77-88.
10. Bhasin M, Wu M, Tsirka SE. 2007. Modulation of microglial/macrophage activation by macrophage inhibitory factor (TKP) or tuftsin (TKPR) attenuates the disease course of experimental autoimmune encephalomyelitis. BMC Immunol 8:10.
11. Bonfoco E, Chen W, Paul R, DA C, Cooper N. 2000. b1 integrin antagonism on adherent, differentiated human neuroblastoma cells triggers an apoptotic signaling pathway. Neuroscience 101:1145-1152.
12. Bruder D, Probst-Kepper M, Westendorf AM, Geffers R, Beissert S, Loser K, von Boehmer H, Buer J, Hansen W. 2004. Neuropilin-1: A surface marker of regulatory T cells. Eur J Immunol 34:623-630.
13. Bystry RS, Aluvihare V, Welch KA, Kallikourdis M, Betz AG. 2001. B cells and professional APCs recruit regulatory T cells via CCL4. Nat Immunol 2:1126-1132.
14. Caito S, Rajendrasozhan S, Cook S, Chung S, Yao H, Friedman AE, Brookes PS, Rahman I. 2010. SIRT1 is a redox-sensitive deacetylase that is post-translationally modified by oxidants and carbonyl stress. FASEB J 24:3145-3159.
15. Centonze D, Muzio L, Rossi S, Cavasinni F, De Chiara V, Bergami A, Musella A, D'Amelio M, Cavallucci V, Martorana A, Bergamaschi A, Cencioni MT, Diamantini A, Butti E, Comi G, Bernardini G, Cecconi F, Battistini L, Furlan R, Martino G. 2009. Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis. J Neurosci 29:3442-3452.
16. Chen W, Jin W, Tian H, Sicurello P, Frank M, Orenstein JM, Wahl SM. 2001. Requirement for transforming growth factor beta1 in controlling T cell apoptosis. J Exp Med 194:439-453.
17. Chen W, Wahl SM. 2003. TGF-beta: The missing link in CD4+CD25+ regulatory T cell-mediated immunosuppression. Cytokine Growth Factor Rev 14:85-89.
18. Chen X, Zhang L, Zhang IY, Liang J, Wang H, Ouyang M, Wu S, da Fonseca AC, Weng L, Yamamoto Y, Yamamoto H, Natarajan R, Badie B. 2014. RAGE expression in tumor-associated macrophages promotes angiogenesis in glioma. Cancer Res 74:7285-7297.
19. Del Pino I, Garcia-Frigola C, Dehorter N, Brotons-Mas JR, Alvarez-Salvado E, Martinez de Lagran M, Ciceri G, Gabaldon MV, Moratal D, Dierssen M, Canals S, Marin O, Rico B. 2013. Erbb4 deletion from fast-spiking interneurons causes schizophrenia-like phenotypes. Neuron 79:1152-1168.
20. Deng L, Zhou JF, Sellers RS, Li JF, Nguyen AV, Wang Y, Orlofsky A, Liu Q, Hume DA, Pollard JW, Augenlicht L, Lin EY. 2010. A novel mouse model of inflammatory bowel disease links mammalian target of rapamycin-dependent hyperproliferation of colonic epithelium to inflammation-associated tumorigenesis. Am J Pathol 176:952-967.
21. Durafourt BA, Moore CS, Zammit DA, Johnson TA, Zaguia F, Guiot MC, Bar-Or A, Antel JP. 2012. Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia 60:717-727.
22. Dustin ML, Bromley SK, Kan Z, Peterson DA, Unanue ER. 1997. Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc Natl Acad Sci USA 94:3909-3913.
23. Ebner F, Brandt C, Thiele P, Richter D, Schliesser U, Siffrin V, Schueler J, Stubbe T, Ellinghaus A, Meisel C, Sawitzki B, Nitsch R. 2013. Microglial activation milieu controls regulatory T cell responses. J Immunol 191:5594-5602.
24. Edwards JP, Zhang X, Frauwirth KA, Mosser DM. 2006. Biochemical and functional characterization of three activated macrophage populations. J Leukoc Biol 80:1298-1307.
25. Emerson MR, Gallagher RJ, Marquis JG, LeVine SM. 2009. Enhancing the ability of experimental autoimmune encephalomyelitis to serve as a more rigorous model of multiple sclerosis through refinement of the experimental design. Comp Med 59:112-128.
26. Fantin A, Vieira JM, Plein A, Denti L, Fruttiger M, Pollard JW, Ruhrberg C. 2013. NRP1 acts cell autonomously in endothelium to promote tip cell function during sprouting angiogenesis. Blood 121:2352-2362.
27. Fletcher JM, Lalor SJ, Sweeney CM, Tubridy N, Mills KH. 2010. T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin Exp Immunol 162:1-11.
28. Fridkin M, Najjar VA. 1989. Tuftsin: Its chemistry, biology, and clinical potential. Crit Rev Biochem Mol Biol 24:1-40.
29. Friedl P, den Boer AT, Gunzer M. 2005. Tuning immune responses: Diversity and adaptation of the immunological synapse. Nat Rev Immunol 5:532-545.
30. Frisancho-Kiss S, Coronado MJ, Frisancho JA, Lau VM, Rose NR, Klein SL, Fairweather D. 2009. Gonadectomy of male BALB/c mice increases Tim-3(+) alternatively activated M2 macrophages, Tim-3(+) T cells, Th2 cells and Treg in the heart during acute coxsackievirus-induced myocarditis. Brain Behav Immun 23:649-657.
31. Gerber JS, Mosser DM. 2001. Reversing lipopolysaccharide toxicity by ligating the macrophage Fc gamma receptors. J Immunol 166:6861-6868.
32. Glinka Y, Prud'homme GJ. 2008. Neuropilin-1 is a receptor for transforming growth factor beta-1, activates its latent form, and promotes regulatory T cell activity. J Leukoc Biol 84:302-310.
33. Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS, Allen PM, Dustin ML. 1999. The immunological synapse: A molecular machine controlling T cell activation. Science 285:221-227.
34. Gu C, Rodriguez ER, Reimert DV, Shu T, Fritzsch B, Richards LJ, Kolodkin AL, Ginty DD. 2003. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Developmental cell 5:45-57.
35. Hjelmstrom P, Juedes AE, Fjell J, Ruddle NH. 1998. B-cell-deficient mice develop experimental allergic encephalomyelitis with demyelination after myelin oligodendrocyte glycoprotein sensitization. J Immunol 161:4480-4483.
36. Hsieh CS, Liang Y, Tyznik AJ, Self SG, Liggitt D, Rudensky AY. 2004. Recognition of the peripheral self by naturally arising CD25+ CD4+ T cell receptors. Immunity 21:267-277.
37. Huber S, Schramm C, Lehr HA, Mann A, Schmitt S, Becker C, Protschka M, Galle PR, Neurath MF, Blessing M. 2004. Cutting edge: TGF-beta signaling is required for the in vivo expansion and immunosuppressive capacity of regulatory CD4+CD25+ T cells. J Immunol 173:6526-6531.
38. Kigerl K, Gensel J, Ankeny D, Alexander J, Donnelly D, Popovich P. 2009. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 29:13435-13444.
39. Kim JM, Rasmussen JP, Rudensky AY. 2007. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol 8:191-197.
40. Kipnis J, Avidan H, Caspi RR, Schwartz M. 2004. Dual effect of CD4+CD25+ regulatory T cells in neurodegeneration: A dialogue with microglia. Proc Natl Acad Sci USA 101:14663-14669.
41. Kohm AP, Carpentier PA, Anger HA, Miller SD. 2002. Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J Immunol 169:4712-4716.
42. Li WW, Setzu A, Zhao C, Franklin RJ. 2005. Minocycline-mediated inhibition of microglia activation impairs oligodendrocyte progenitor cell responses and remyelination in a non-immune model of demyelination. J Neuroimmunol 158:58-66.
43. Liu Y, Jiang J, Xiao H, Wang X, Li Y, Gong Y, Huang Y. 2012. The sphingosine-1-phosphate receptor agonist FTY720 and its phosphorylated form affect the function of CD4+CD25+ T cells in vitro. Int J Mol Med 30:211-219.
44. Majed H, Chandran S, Niclou S, Nicholas R, Wilkins A, Wing M, Rhodes K, Spillantini M, Compston A. 2006. A novel role for Sema3A in neuroprotection from injury mediated by activated microglia. J Neurosci 26:1730-1738.
45. Matta SG, Balfour DJ, Benowitz NL, Boyd RT, Buccafusco JJ, Caggiula AR, Craig CR, Collins AC, Damaj MI, Donny EC, Gardiner PS, Grady SR, Heberlein U, Leonard SS, Levin ED, Lukas RJ, Markou A, Marks MJ, McCallum SE, Parameswaran N, Perkins KA, Piccioto MR, Quik M, Rose JE, Rothenfluh A, Schafer WR, Stolerman IP, Tyndale RF, Wehner JM, Zirger JM. 2007. Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190:269-319.
46. McMenamin PG. 1999. Distribution and phenotype of dendritic cells and resident tissue macrophages in the dura mater, leptomeninges, and choroid plexus of the rat brain as demonstrated in wholemount preparations. J Comp Neurol 405:553-562.
47. Mikita J, Dubourdieu-Cassagno N, Deloire MS, Vekris A, Biran M, Raffard G, Brochet B, Canron MH, Franconi JM, Boiziau C, Petry KG. 2011. Altered M1/M2 activation patterns of monocytes in severe relapsing experimental rat model of multiple sclerosis. Amelioration of clinical status by M2 activated monocyte administration. Mult Scler 17:2-15.
48. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM. 2000. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 164:6166-6173.
49. Miron VE, Boyd A, Zhao JW, Yuen TJ, Ruckh JM, Shadrach JL, van Wijngaarden P, Wagers AJ, Williams A, Franklin RJ, ffrench-Constant C. 2013. M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat Neurosci 16:1211-1218.
50. Miyara M, Sakaguchi S. 2007. Natural regulatory T cells: Mechanisms of suppression. Trends Mol Med 13:108-116.
51. Neumann H, Kotter MR, Franklin RJ. 2009. Debris clearance by microglia: An essential link between degeneration and regeneration. Brain 132:288-295.
52. Nissen JC, Selwood DL, Tsirka SE. 2013. Tuftsin signals through its receptor neuropilin-1 via the transforming growth factor beta pathway. J Neurochem 127:394-402.
53. Olmos-Serrano JL, Paluszkiewicz SM, Martin BS, Kaufmann WE, Corbin JG, Huntsman MM. 2010. Defective GABAergic neurotransmission and pharmacological rescue of neuronal hyperexcitability in the amygdala in a mouse model of fragile X syndrome. J Neurosci 30:9929-9938.
54. Olson JK, Girvin AM, Miller SD. 2001. Direct activation of innate and antigen-presenting functions of microglia following infection with Theiler's virus. J Virol 75:9780-9789.
55. Perdiguero EG, Klapproth K, Schulz C, Busch K, Azzoni E, Crozet L, Garner H, Trouillet C, de Bruijn MF, Geissmann F, Rodewald HR. 2015. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518:547-551.
56. Raivich G, Banati R. 2004. Brain microglia and blood-derived macrophages: Molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease. Brain Res Brain Res Rev 46:261-281.
57. Reddy J, Illes Z, Zhang X, Encinas J, Pyrdol J, Nicholson L, Sobel RA, Wucherpfennig KW, Kuchroo VK. 2004. Myelin proteolipid protein-specific CD4+CD25+ regulatory cells mediate genetic resistance to experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 101:15434-15439.
58. Reynolds AD, Banerjee R, Liu J, Gendelman HE, Mosley RL. 2007. Neuroprotective activities of CD4+CD25+ regulatory T cells in an animal model of Parkinson's disease. J Leukoc Biol 82:1083-1094.
59. Rogove A, Siao C, Keyt B, Strickland S, Tsirka S. 1999. Activation of microglia reveals a non-proteolytic cytokine function for tissue plasminogen activator in the central nervous system. J Cell Sci 112:4007-4016.
60. Rogove AD, Tsirka SE. 1998. Neurotoxic responses by microglia elicited by excitotoxic injury in the mouse hippocampus. Curr Biol 8:19-25.
61. Sagar D, Lamontagne A, Foss CA, Khan ZK, Pomper MG, Jain P. 2012. Dendritic cell CNS recruitment correlates with disease severity in EAE via CCL2 chemotaxis at the blood-brain barrier through paracellular transmigration and ERK activation. J Neuroinflamm 9:245.
62. Sarris M, Andersen K, Randow F, Mayr L, Betz A. 2008. Neuropilin-1 expression on regulatory T cells enhances their interactions with dendritic cells during antigen recognition. Immunity 28:402-413.
63. Siao CJ, Tsirka SE. 2002. Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II. J Neurosci 22:3352-3358.
64. Siemion IZ, Kluczyk A. 1999. Tuftsin: On the 30-year anniversary of Victor Najjar's discovery. Peptides 20:645-674.
65. Silver D, Livingston D. 2001. Self-excising retroviral vectors encoding the Cre recombinase overcome Cre-mediated cellular toxicity. Mol Cell 8:233-243.
66. Solomon BD, Mueller C, Chae WJ, Alabanza LM, Bynoe MS. 2011. Neuropilin-1 attenuates autoreactivity in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 108:2040-2045.
67. Swanborg RH. 1995. Experimental autoimmune encephalomyelitis in rodents as a model for human demyelinating disease. Clin Immunol Immunopathol 77:4-13.
68. Tarbell KV, Yamazaki S, Steinman RM. 2006. The interactions of dendritic cells with antigen-specific, regulatory T cells that suppress autoimmunity. Semin Immunol 18:93-102.
69. Tordjman R, Lepelletier Y, Lemarchandel V, Cambot M, Gaulard P, Hermine O, Roméo P. 2002. A neuronal receptor, neuropilin-1, is essential for the initiation of the primary immune response. Nat Immunol 3:477-482.
70. Tzehoval E, Segal S, Stabinsky Y, Fridkin M, Spirer Z, Feldman M. 1978. Tuftsin (an Ig-associated tetrapeptide) triggers the immunogenic function of macrophages: Implications for activation of programmed cells. Proc Natl Acad Sci USA 75:3400-3404.
71. Wlodarczyk A, Lobner M, Cedile O, Owens T. 2014. Comparison of microglia and infiltrating CD11c(+) cells as antigen presenting cells for T cell proliferation and cytokine response. J Neuroinflammation 11:57.
72. Wu M, Nissen JC, Chen EI, Tsirka SE. 2012. Tuftsin promotes an anti-inflammatory switch and attenuates symptoms in experimental autoimmune encephalomyelitis. PLoS One 7:e34933.
73. Xie L, Choudhury GR, Winters A, Yang SH, Jin K. 2015. Cerebral regulatory T cells restrain microglia/macrophage-mediated inflammatory responses via IL-10. Eur J Immunol 45:180-191.
74. Yang Z, Yu A, Liu Y, Shen H, Lin C, Lin L, Wang S, Yuan B. 2014. Regulatory T cells inhibit microglia activation and protect against inflammatory injury in intracerebral hemorrhage. Int Immunopharmacol 22:522-525.