Immune Regulation of Antibody Access to Neuronal Tissues

Trends in Molecular Medicine

Volumn 23, Issue 3, 2017, Pages 227-245

  Iwasaki, Akiko ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; IMMUNOMODULATING AGENT; INTERFERON; PROTEIN TYROSINE KINASE;

ADAPTIVE IMMUNITY; BLOOD BRAIN BARRIER; BLOOD NERVE BARRIER; BRAIN TUMOR; CANCER IMMUNOTHERAPY; CENTRAL NERVOUS SYSTEM; DEGENERATIVE DISEASE; HUMAN; IMMUNOREGULATION; IMMUNOSURVEILLANCE; INNATE IMMUNITY; MULTICENTER STUDY (TOPIC); NERVOUS TISSUE; NEUROPROTECTION; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; T LYMPHOCYTE; VIRUS; ANIMAL; BRAIN NEOPLASMS; IMMUNOLOGY; IMMUNOTHERAPY; NEURODEGENERATIVE DISEASES; PATHOLOGY; VIROLOGY; VIRUS INFECTION;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES; BLOOD-BRAIN BARRIER; BLOOD-NERVE BARRIER; BRAIN NEOPLASMS; HUMANS; IMMUNITY, INNATE; IMMUNOTHERAPY; INTERFERONS; NEURODEGENERATIVE DISEASES; RECEPTOR PROTEIN-TYROSINE KINASES; T-LYMPHOCYTES; VIRUS DISEASES; VIRUSES;

EID: 85011588269     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2017.01.004     Document Type: Review

References (102)

1. 1 Gunn, B.M., Alter, G., Modulating antibody functionality in infectious disease and vaccination. Trends Mol. Med. 22 (2016), 969–982.
2. 2 Iwasaki, A., Exploiting mucosal immunity for antiviral vaccines. Annu. Rev. Immunol. 34 (2016), 575–608.
3. 3 Roopenian, D.C., Akilesh, S., FcRn: the neonatal Fc receptor comes of age. Nat. Rev. Immunol. 7 (2007), 715–725.
4. 4 Story, C.M., et al. A major histocompatibility complex class I-like Fc receptor cloned from human placenta: possible role in transfer of immunoglobulin G from mother to fetus. J. Exp. Med. 180 (1994), 2377–2381.
5. 5 Zhao, Z., et al. Establishment and dysfunction of the blood–brain barrier. Cell 163 (2015), 1064–1078.
6. 6 Schlager, C., et al. Effector T-cell trafficking between the leptomeninges and the cerebrospinal fluid. Nature 530 (2016), 349–353.
7. 7 Arima, Y., et al. Regional neural activation defines a gateway for autoreactive T cells to cross the blood–brain barrier. Cell 148 (2012), 447–457.
8. 8 Arima, Y., et al. A pain-mediated neural signal induces relapse in murine autoimmune encephalomyelitis, a multiple sclerosis model. Elife, 4, 2015, 08733.
9. 9 Reboldi, A., et al. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 10 (2009), 514–523.
10. + T-cell help. Nature 533 (2016), 552–556.
11. 11 Sevigny, J., et al. The antibody aducanumab reduces Abeta plaques in Alzheimer's disease. Nature 537 (2016), 50–56.
12. 12 Engelhardt, B., Ransohoff, R.M., Capture, crawl, cross: the T cell code to breach the blood–brain barriers. Trends Immunol. 33 (2012), 579–589.
13. 13 Weerasuriya, A., Mizisin, A.P., The blood–nerve barrier: structure and functional significance. Methods Mol. Biol. 686 (2011), 149–173.
14. 14 Corfas, G., et al. Mechanisms and roles of axon–Schwann cell interactions. J. Neurosci. 24 (2004), 9250–9260.
15. 15 Obermeier, B., et al. Development, maintenance and disruption of the blood–brain barrier. Nat. Med. 19 (2013), 1584–1596.
16. 16 Daneman, R., et al. Pericytes are required for blood–brain barrier integrity during embryogenesis. Nature 468 (2010), 562–566.
17. 17 Ben-Zvi, A., et al. Mfsd2a is critical for the formation and function of the blood–brain barrier. Nature 509 (2014), 507–511.
18. 18 Saunders, N.R., et al. Barrier mechanisms in the developing brain. Front. Pharmacol., 3, 2012, 46.
19. 19 Braniste, V., et al. The gut microbiota influences blood–brain barrier permeability in mice. Sci. Transl. Med., 6, 2014, 263ra158.
20. 20 Rochfort, K.D., Cummins, P.M., The blood–brain barrier endothelium: a target for pro-inflammatory cytokines. Biochem. Soc. Trans. 43 (2015), 702–706.
21. 21 Daniels, B.P., et al. Viral pathogen-associated molecular patterns regulate blood–brain barrier integrity via competing innate cytokine signals. MBio 5 (2014), 14–e01476.
22. 22 Lazear, H.M., et al. Interferon-lambda restricts West Nile virus neuroinvasion by tightening the blood–brain barrier. Sci. Transl. Med., 7, 2015, 284ra59.
23. 23 Miner, J.J., et al. The TAM receptor Mertk protects against neuroinvasive viral infection by maintaining blood–brain barrier integrity. Nat. Med. 21 (2015), 1464–1472.
24. 24 Zhu, D., et al. Protein S controls hypoxic/ischemic blood–brain barrier disruption through the TAM receptor Tyro3 and sphingosine 1-phosphate receptor. Blood 115 (2010), 4963–4972.
25. 25 Ransohoff, R.M., Brown, M.A., Innate immunity in the central nervous system. J. Clin. Invest. 122 (2012), 1164–1171.
26. 26 Schoggins, J.W., Rice, C.M., Interferon-stimulated genes and their antiviral effector functions. Curr. Opin. Virol. 1 (2011), 519–525.
27. 27 Veldhuis, W.B., et al. Interferon-beta prevents cytokine-induced neutrophil infiltration and attenuates blood–brain barrier disruption. J. Cereb. Blood Flow Metab., 23, 2003 1060-1-69.
28. 28 Lemke, G., Rothlin, C.V., Immunobiology of the TAM receptors. Nat. Rev. Immunol. 8 (2008), 327–336.
29. 29 Lew, E.D., et al. Differential TAM receptor–ligand–phospholipid interactions delimit differential TAM bioactivities. Elife, 3, 2014, 03385.
30. 30 Rothlin, C.V., et al. TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 131 (2007), 1124–1136.
31. 31 Ma, G.Z., et al. Polymorphisms in the receptor tyrosine kinase MERTK gene are associated with multiple sclerosis susceptibility. PLoS One, 6, 2011, e16964.
32. 32 Sawcer, S., et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476 (2011), 214–219.
33. 33 Australia and New Zealand Multiple Sclerosis Genetics Consortium (ANZgene), Genome-wide association study identifies new multiple sclerosis susceptibility loci on chromosomes 12 and 20. Nat. Genet. 41 (2009), 824–828.
34. 34 Bruewer, M., et al. Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J. 19 (2005), 923–933.
35. 35 Utech, M., et al. Mechanism of IFN-gamma-induced endocytosis of tight junction proteins: myosin II-dependent vacuolarization of the apical plasma membrane. Mol. Biol. Cell 16 (2005), 5040–5052.
36. 36 Kebir, H., et al. Human TH17 lymphocytes promote blood–brain barrier disruption and central nervous system inflammation. Nat. Med. 13 (2007), 1173–1175.
37. 37 Carrithers, M.D., et al. Differential adhesion molecule requirements for immune surveillance and inflammatory recruitment. Brain 123 (2000), 1092–1101.
38. 38 Springer, T.A., Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76 (1994), 301–314.
39. 39 Pober, J.S., Sessa, W.C., Evolving functions of endothelial cells in inflammation. Nat. Rev. Immunol. 7 (2007), 803–815.
40. 40 Muller, W.A., How endothelial cells regulate transmigration of leukocytes in the inflammatory response. Am. J. Pathol. 184 (2014), 886–896.
41. 41 Ransohoff, R.M., et al. Three or more routes for leukocyte migration into the central nervous system. Nat. Rev. Immunol. 3 (2003), 569–581.
42. + T cells: evidence for trafficking through choroid plexus and meninges via P-selectin. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 8389–8394.
43. + T cells is required for their entry into brain parenchyma. J. Exp. Med. 177 (1993), 57–68.
44. 44 Baron, J.L., et al. The pathogenesis of adoptive murine autoimmune diabetes requires an interaction between alpha 4-integrins and vascular cell adhesion molecule-1. J. Clin. Invest. 93 (1994), 1700–1708.
45. 45 Lee, S.J., Benveniste, E.N., Adhesion molecule expression and regulation on cells of the central nervous system. J. Neuroimmunol. 98 (1999), 77–88.
46. 46 Linington, C., et al. Augmentation of demyelination in rat acute allergic encephalomyelitis by circulating mouse monoclonal antibodies directed against a myelin/oligodendrocyte glycoprotein. Am. J. Pathol. 130 (1988), 443–454.
47. 47 Kojima, K., et al. Experimental autoimmune panencephalitis and uveoretinitis transferred to the Lewis rat by T lymphocytes specific for the S100 beta molecule, a calcium binding protein of astroglia. J. Exp. Med. 180 (1994), 817–829.
48. 48 Westland, K.W., et al. Activated non-neural specific T cells open the blood–brain barrier to circulating antibodies. Brain 122 (1999), 1283–1291.
49. 49 Miner, J.J., Diamond, M.S., Mechanisms of restriction of viral neuroinvasion at the blood–brain barrier. Curr. Opin. Immunol. 38 (2016), 18–23.
50. 50 Koyuncu, O.O., et al. Virus infections in the nervous system. Cell Host Microbe 13 (2013), 379–393.
51. 51 Dittmar, S., et al. Measles virus-induced block of transendothelial migration of T lymphocytes and infection-mediated virus spread across endothelial cell barriers. J. Virol. 82 (2008), 11273–11282.
52. 52 Plakhov, I.V., et al. The earliest events in vesicular stomatitis virus infection of the murine olfactory neuroepithelium and entry of the central nervous system. Virology 209 (1995), 257–262.
53. 53 Verma, S., et al. West Nile virus infection modulates human brain microvascular endothelial cells tight junction proteins and cell adhesion molecules: transmigration across the in vitro blood–brain barrier. Virology 385 (2009), 425–433.
54. 54 Wang, S., et al. Drak2 contributes to West Nile virus entry into the brain and lethal encephalitis. J. Immunol. 181 (2008), 2084–2091.
55. 55 Li, F., et al. Viral infection of the central nervous system and neuroinflammation precede blood–brain barrier disruption during Japanese encephalitis virus Infection. J. Virol. 89 (2015), 5602–5614.
56. 56 Cook, M.L., Stevens, J.G., Pathogenesis of herpetic neuritis and ganglionitis in mice: evidence for intra-axonal transport of infection. Infect. Immun. 7 (1973), 272–288.
57. 57 Racaniello, V.R., One hundred years of poliovirus pathogenesis. Virology 344 (2006), 9–16.
58. 58 Koelle, D.M., Corey, L., Herpes simplex: insights on pathogenesis and possible vaccines. Annu. Rev. Med. 59 (2008), 381–395.
59. 59 Whaley, K.J., et al. Passive immunization of the vagina protects mice against vaginal transmission of genital herpes infections. J. Infect. Dis. 169 (1994), 647–649.
60. 60 Sherwood, J.K., et al. Controlled release of antibodies for long-term topical passive immunoprotection of female mice against genital herpes. Nat. Biotechnol. 14 (1996), 468–471.
61. 61 Faden, H., et al. Comparative evaluation of immunization with live attenuated and enhanced-potency inactivated trivalent poliovirus vaccines in childhood: systemic and local immune responses. J. Infect. Dis. 162 (1990), 1291–1297.
62. 62 Morrison, L.A., et al. Vaccine-induced serum immunoglobin contributes to protection from herpes simplex virus type 2 genital infection in the presence of immune T cells. J. Virol. 75 (2001), 1195–1204.
63. 63 Sato, A., et al. Vaginal memory T cells induced by intranasal vaccination are critical for protective T cell recruitment and prevention of genital HSV-2 disease. J. Virol. 88 (2014), 13699–13708.
64. 64 Parr, M.B., Parr, E.L., Interferon-gamma up-regulates intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 and recruits lymphocytes into the vagina of immune mice challenged with herpes simplex virus-2. Immunology 99 (2000), 540–545.
65. 65 Hooper, D.C., et al. Collaboration of antibody and inflammation in clearance of rabies virus from the central nervous system. J. Virol. 72 (1998), 3711–3719.
66. 66 Chai, Q., et al. Enhancement of blood–brain barrier permeability and reduction of tight junction protein expression are modulated by chemokines/cytokines induced by rabies virus infection. J. Virol. 88 (2014), 4698–4710.
67. 67 Ortiz, G.G., et al. Role of the blood–brain barrier in multiple sclerosis. Arch. Med. Res. 45 (2014), 687–697.
68. 68 Brosnan, C.F., et al. Mechanisms of autoimmune neuropathies. Ann. Neurol. 27:Suppl (1990), S75–79.
69. 69 van den Berg, B., et al. Guillain–Barré syndrome: pathogenesis, diagnosis, treatment and prognosis. Nat. Rev. Neurol. 10 (2014), 469–482.
70. 70 Gilden, D.H., Infectious causes of multiple sclerosis. Lancet Neurol. 4 (2005), 195–202.
71. 71 Gaublomme, J.T., et al. Single-cell genomics unveils critical regulators of Th17 cell pathogenicity. Cell 163 (2015), 1400–1412.
72. 72 Polman, C.H., et al. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N. Engl. J. Med. 354 (2006), 899–910.
73. 73 Bloomgren, G., et al. Risk of natalizumab-associated progressive multifocal leukoencephalopathy. N. Engl. J. Med. 366 (2012), 1870–1880.
74. 74 Fraussen, J., et al. B cells and antibodies in progressive multiple sclerosis: contribution to neurodegeneration and progression. Autoimmun. Rev. 15 (2016), 896–899.
75. 75 Latov, N., Diagnosis and treatment of chronic acquired demyelinating polyneuropathies. Nat. Rev. Neurol. 10 (2014), 435–446.
76. 76 Rubenstein, J.L., et al. Rituximab therapy for CNS lymphomas: targeting the leptomeningeal compartment. Blood 101 (2003), 466–468.
77. 77 Bloom, G.S., Amyloid-beta and tau: the trigger and bullet in Alzheimer disease pathogenesis. JAMA Neurol. 71 (2014), 505–508.
78. 78 Agadjanyan, M.G., et al. A fresh perspective from immunologists and vaccine researchers: active vaccination strategies to prevent and reverse Alzheimer's disease. Alzheimers Dement. 11 (2015), 1246–1259.
79. 79 Schenk, D., Amyloid-beta immunotherapy for Alzheimer's disease: the end of the beginning. Nat. Rev. Neurosci. 3 (2002), 824–828.
80. 80 Nicoll, J.A., et al. Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: a case report. Nat. Med. 9 (2003), 448–452.
81. 81 Orgogozo, J.M., et al. Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 61 (2003), 46–54.
82. 82 Ferrer, I., et al. Neuropathology and pathogenesis of encephalitis following amyloid-beta immunization in Alzheimer's disease. Brain Pathol. 14 (2004), 11–20.
83. 83 Sterner, R.M., et al. Active vaccines for Alzheimer disease treatment. J. Am. Med. Dir. Assoc. 17 (2016), 862.e11–862.e15.
84. 84 Vandenberghe, R., et al. Bapineuzumab for mild to moderate Alzheimer's disease in two global, randomized, phase 3 trials. Alzheimers Res. Ther., 8, 2016, 18.
85. 85 Salloway, S., et al. Two phase 3 trials of bapineuzumab in mild-to-moderate Alzheimer's disease. N. Engl. J. Med. 370 (2014), 322–333.
86. 86 Siemers, E.R., et al. Phase 3 solanezumab trials: secondary outcomes in mild Alzheimer's disease patients. Alzheimers Dement. 12 (2016), 110–120.
87. 87 Ferenczy, M.W., et al. Molecular biology, epidemiology, and pathogenesis of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clin. Microbiol. Rev. 25 (2012), 471–506.
88. 88 Jaeger, L.B., et al. Testing the neurovascular hypothesis of Alzheimer's disease: LRP-1 antisense reduces blood–brain barrier clearance, increases brain levels of amyloid-beta protein, and impairs cognition. J. Alzheimers Dis. 17 (2009), 553–570.
89. 89 Tsutsui, Y., et al. Roles of neural stem progenitor cells in cytomegalovirus infection of the brain in mouse models. Pathol. Int. 58 (2008), 257–267.
90. 90 Chaturvedi, U.C., et al. Breakdown of the blood–brain barrier during dengue virus infection of mice. J. Gen. Virol. 72 (1991), 859–866.
91. 91 An, J., et al. The pathogenesis of spinal cord involvement in dengue virus infection. Virchows Arch. 442 (2003), 472–481.
92. 92 Zerboni, L., et al. Molecular mechanisms of varicella zoster virus pathogenesis. Nat. Rev. Microbiol. 12 (2014), 197–210.
93. 93 Roe, K., et al. West Nile virus-induced disruption of the blood–brain barrier in mice is characterized by the degradation of the junctional complex proteins and increase in multiple matrix metalloproteinases. J. Gen.Virol. 93 (2012), 1193–1203.
94. 94 Miner, J.J., et al. Zika virus infection during pregnancy in mice causes placental damage and fetal demise. Cell 165 (2016), 1081–1091.
95. 95 Li, C., et al. Zika virus disrupts neural progenitor development and leads to microcephaly in mice. Cell Stem Cell 19 (2016), 120–126.
96. 96 Dang, J., et al. Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor TLR3. Cell Stem Cell 19 (2016), 258–265.
97. 97 Tang, H., et al. Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell 18 (2016), 587–590.
98. 98 Garcez, P.P., et al. Zika virus impairs growth in human neurospheres and brain organoids. Science 352 (2016), 816–818.
99. 99 Qian, X., et al. Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165 (2016), 1238–1254.
100. 100 Yockey, L.J., et al. Vaginal exposure to Zika virus during pregnancy leads to fetal brain infection. Cell 166 (2016), 1247–1256.
101. 101 Li, H., et al. Zika virus infects neural progenitors in the adult mouse brain and alters proliferation. Cell Stem Cell 19 (2016), 593–598.
102. 102 Onorati, M., et al. Zika virus disrupts phospho-TBK1 localization and mitosis in human neuroepithelial stem cells and radial glia. Cell Rep. 16 (2016), 2576–2592.