Enhancement of blood-brain barrier permeability is required for intravenously administered virus neutralizing antibodies to clear an established rabies virus infection from the brain and prevent the development of rabies in mice

Antiviral Research

Volumn 110, Issue , 2014, Pages 132-141

  Huang, Chien Tsun ^a   Li, Zhenguang ^a,b   Huang, Ying ^a   Zhang, Guoqing ^a   Zhou, Ming ^a   Chai, Qingqing ^a   Wu, Hua ^b   Fu, Zhen F ^a,c  

^a UNIVERSITY OF GEORGIA   (United States)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

BBB (blood brain barrier); Claudin 5; MCP 1; Occludin; Rabies virus; VNA (virus neutralizing antibody)

Indexed keywords

ANTISERUM; CCL2 PROTEIN, MOUSE; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY; BETA ACTIN; CLAUDIN 5; IMMUNOGLOBULIN KAPPA CHAIN; MESSENGER RNA; OCCLUDIN;

ANIMAL; B LYMPHOCYTE; BLOOD BRAIN BARRIER; BRAIN; DRUG EFFECTS; FEMALE; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; MOUSE; PASSIVE IMMUNIZATION; PATHOGENICITY; PERMEABILITY; PHYSIOLOGY; RABIES; RABIES VIRUS; TIGHT JUNCTION; TRANSPORT AT THE CELLULAR LEVEL; VIROLOGY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY DETECTION; ARTICLE; DOWN REGULATION; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; VIRAL CLEARANCE; VIRUS TITRATION; WESTERN BLOTTING; WILD TYPE;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; B-LYMPHOCYTES; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; CHEMOKINE CCL2; FEMALE; IMMUNE SERA; IMMUNIZATION, PASSIVE; MICE; MICE, INBRED ICR; PERMEABILITY; RABIES; RABIES VIRUS; TIGHT JUNCTIONS;

MUS; RABIES VIRUS;

EID: 84906923687     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2014.07.013     Document Type: Article

References (64)

1. N.J. Abbott, A.A. Patabendige, D.E. Dolman, S.R. Yusof, and D.J. Begley Structure and function of the blood-brain barrier Neurobiol. Dis. 37 2010 13 25
2. S.M. Armstrong, C. Wang, J. Tigdi, X. Si, C. Dumpit, S. Charles, A. Gamage, T.J. Moraes, and W.L. Lee Influenza infects lung microvascular endothelium leading to microvascular leak: role of apoptosis and claudin-5 PLoS One 7 2012 e47323
3. P. Ballabh, A. Braun, and M. Nedergaard The blood-brain barrier: an overview: structure, regulation, and clinical implications Neurobiol. Dis. 16 2004 1 13
4. M. Baltazard, and M. Ghodssi Prevention of human rabies: treatment of persons bitten by rabid wolves in Iran Bull. World Health Organ. 10 1954 797 803
5. V. Braniste, M. Leveque, C. Buisson-Brenac, L. Bueno, J. Fioramonti, and E. Houdeau Oestradiol decreases colonic permeability through oestrogen receptor beta-mediated up-regulation of occludin and junctional adhesion molecule-A in epithelial cells J. Physiol. 587 2009 3317 3328
6. B. Brochier, M.P. Kieny, F. Costy, P. Coppens, B. Bauduin, J.P. Lecocq, B. Languet, G. Chappuis, P. Desmettre, and K. Afiademanyo et al. Large-scale eradication of rabies using recombinant vaccinia-rabies vaccine Nature 354 1991 520 522
7. CDC, 2010. Use of a Reduced (4-Dose) Vaccine Schedule for Postexposure Prophylaxis to Prevent Human Rabies. MMWR 59.
8. Q. Chai, W.Q. He, M. Zhou, H. Lu, and Z.F. Fu 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
9. S. Cleaveland, M. Kaare, D. Knobel, and M.K. Laurenson Canine vaccination - providing broader benefits for disease control Vet. Microbiol. 117 2006 43 50
10. B. Dietzschold, K. Morimoto, D.C. Hooper, J.S. Smith, C.E. Rupprecht, and H. Koprowski Genotypic and phenotypic diversity of rabies virus variants involved in human rabies: implications for postexposure prophylaxis J. Hum. Virol. 3 2000 50 57
11. M. Faber, R. Pulmanausahakul, S.S. Hodawadekar, S. Spitsin, J.P. McGettigan, M.J. Schnell, and B. Dietzschold Overexpression of the rabies virus glycoprotein results in enhancement of apoptosis and antiviral immune response J. Virol. 76 2002 3374 3381
12. M. Faber, J. Li, R.B. Kean, D.C. Hooper, K.R. Alugupalli, and B. Dietzschold Effective preexposure and postexposure prophylaxis of rabies with a highly attenuated recombinant rabies virus Proc. Natl. Acad. Sci. USA 106 2009 11300 11305
13. S.R. Favoretto, M.L. Carrieri, M.S. Tino, C.R. Zanetti, and O.A. Pereira Simplified fluorescent inhibition microtest for the titration of rabies neutralizing antibodies Rev. Inst. Med. Trop. Sao Paulo 35 1993 171 175
14. D.E. Griffin Immune responses to RNA-virus infections of the CNS Nat. Rev. Immunol. 3 2003 493 502
15. K. Hampson, J. Dushoff, S. Cleaveland, D.T. Haydon, M. Kaare, C. Packer, and A. Dobson Transmission dynamics and prospects for the elimination of canine rabies PLoS Biol. 7 2009 e53
16. C.A. Hanlon, M. Niezgoda, A.N. Hamir, C. Schumacher, H. Koprowski, and C.E. Rupprecht First North American field release of a vaccinia-rabies glycoprotein recombinant virus J. Wildl. Dis. 34 1998 228 239
17. T. Hemachudha Human rabies: clinical aspects, pathogenesis, and potential therapy Curr. top. microbio. 187 1994 121 143
18. T. Hemachudha, B. Sunsaneewitayakul, T. Desudchit, C. Suankratay, C. Sittipunt, S. Wacharapluesadee, P. Khawplod, H. Wilde, and A.C. Jackson Failure of therapeutic coma and ketamine for therapy of human rabies J. Neurovirol. 12 2006 407 409
19. D.C. Hooper The role of immune responses in the pathogenesis of rabies J. Neurovirol. 11 2005 88 92
20. D.C. Hooper, T.W. Phares, M.J. Fabis, and A. Roy The production of antibody by invading B cells is required for the clearance of rabies virus from the central nervous system PLoS Negl. Trop. Dis. 3 2009 e535
21. M.P. Hosking, and T.E. Lane The role of chemokines during viral infection of the CNS PLoS Pathog. 6 2010 e1000937
22. A.C. Jackson Rabies pathogenesis J. Neurovirol. 8 2002 267 269
23. A.C. Jackson Current and future approaches to the therapy of human rabies Antiviral Res. 99 2013 61 67
24. A.C. Jackson Rabies: Scientific Basis of the Disease and its Management third ed. 2013 Academic Press
25. J.V. Kim, S.S. Kang, M.L. Dustin, and D.B. McGavern Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis Nature 457 2009 191 195
26. J. Kirk, J. Plumb, M. Mirakhur, and S. McQuaid Tight junctional abnormality in multiple sclerosis white matter affects all calibres of vessel and is associated with blood-brain barrier leakage and active demyelination J. Pathol. 201 2003 319 327
27. U. Kniesel, and H. Wolburg Tight junctions of the blood-brain barrier Cell. Mol. Neurobiol. 20 2000 57 76
28. D.L. Knobel, S. Cleaveland, P.G. Coleman, E.M. Fevre, M.I. Meltzer, M.E. Miranda, A. Shaw, J. Zinsstag, and F.X. Meslin Re-evaluating the burden of rabies in Africa and Asia Bull. World Health Organ. 83 2005 360 368
29. Y. Kuang, S.N. Lackay, L. Zhao, and Z.F. Fu Role of chemokines in the enhancement of BBB permeability and inflammatory infiltration after rabies virus infection Virus Res. 144 2009 18 26
30. P.H. Liao, H.H. Yang, P.T. Chou, M.H. Wang, P.C. Chu, H.L. Liu, and L.K. Chen Sufficient virus-neutralizing antibody in the central nerve system improves the survival of rabid rats J. Biomed. Sci. 19 2012 61
31. M.T. Lin, D.R. Hinton, N.W. Marten, C.C. Bergmann, and S.A. Stohlman Antibody prevents virus reactivation within the central nervous system J. Immunol. 162 1999 7358 7368
32. C.P. Marques, P. Kapil, D.R. Hinton, C. Hindinger, S.L. Nutt, R.M. Ransohoff, T.W. Phares, S.A. Stohlman, and C.C. Bergmann CXCR3-dependent plasma blast migration to the central nervous system during viral encephalomyelitis J. Virol. 85 2011 6136 6147
33. L. Martinez Global infectious disease surveillance Int. J. Infect. Dis. 4 2000 222 228
34. R.C. McDermid, L. Saxinger, B. Lee, J. Johnstone, R.T. Gibney, M. Johnson, and S.M. Bagshaw Human rabies encephalitis following bat exposure: failure of therapeutic coma CMAJ 178 2008 557 561
35. MCW, 2009. The Milwaukee Rabies Protocol, Version 3.1. .
36. F.X. Meslin, D.B. Fishbein, and H.C. Matter Rationale and prospects for rabies elimination in developing countries Curr. Top. Microbiol. Immunol. 187 1994 1 26
37. S.L. Messenger, J.S. Smith, L.A. Orciari, P.A. Yager, and C.E. Rupprecht Emerging pattern of rabies deaths and increased viral infectivity Emerg. Infect. Dis. 9 2003 151 154
38. K. Morimoto, M. Patel, S. Corisdeo, D.C. Hooper, Z.F. Fu, C.E. Rupprecht, H. Koprowski, and B. Dietzschold Characterization of a unique variant of bat rabies virus responsible for newly emerging human cases in North America Proc. Natl. Acad. Sci. USA 93 1996 5653 5658
39. E.A. Neuwelt Mechanisms of disease: the blood-brain barrier Neurosurgery 54 2004 131 140 discussion 141-132
40. T.W. Phares, R.B. Kean, T. Mikheeva, and D.C. Hooper Regional differences in blood-brain barrier permeability changes and inflammation in the apathogenic clearance of virus from the central nervous system J. Immunol. 176 2006 7666 7675
41. T.W. Phares, M.J. Fabis, C.M. Brimer, R.B. Kean, and D.C. Hooper A peroxynitrite-dependent pathway is responsible for blood-brain barrier permeability changes during a central nervous system inflammatory response: TNF-alpha is neither necessary nor sufficient J. Immunol. 178 2007 7334 7343
42. T.W. Phares, S.A. Stohlman, and C.C. Bergmann Intrathecal humoral immunity to encephalitic RNA viruses Viruses 5 2013 732 752
43. C. Ramakrishna, C.C. Bergmann, R. Atkinson, and S.A. Stohlman Control of central nervous system viral persistence by neutralizing antibody J. Virol. 77 2003 4670 4678
44. L.J. Reed, and H. Muench A simple method of estimating fifty per cent endpoints Am. J. Epidemiol. 27 1938 493 497
45. A. Roy, and D.C. Hooper Lethal silver-haired bat rabies virus infection can be prevented by opening the blood-brain barrier J. Virol. 81 2007 7993 7998
46. A. Roy, and D.C. Hooper Immune evasion by rabies viruses through the maintenance of blood-brain barrier integrity J. Neurovirol. 14 2008 401 411
47. A. Roy, T.W. Phares, H. Koprowski, and D.C. Hooper Failure to open the blood-brain barrier and deliver immune effectors to central nervous system tissues leads to the lethal outcome of silver-haired bat rabies virus infection J. Virol. 81 2007 1110 1118
48. C.E. Rupprecht Rhabdoviruses: rabies virus S. Baron, Medical Microbiology fourth ed. 1996 University of Texas Medical Branch at Galveston 751 760
49. C.E. Rupprecht, C.A. Hanlon, and T. Hemachudha Rabies re-examined Lancet Infect. Dis 2 2002 327 343
50. G. Sampath, S. Parikh, P. Sangram, and D.J. Briggs Rabies post-exposure prophylaxis in malnourished children exposed to suspect rabid animals Vaccine 23 2005 1102 1105
51. C.L. Schumacher, P. Coulon, F. Lafay, J. Benejean, M.F. Aubert, J. Barrat, A. Aubert, and A. Flamand SAG-2 oral rabies vaccine Onderstepoort J. Vet. Res. 60 1993 459 462
52. K.R. Spindler, and T.H. Hsu Viral disruption of the blood-brain barrier Trends Microbiol. 20 2012 282 290
53. S.M. Stamatovic, R.F. Keep, S.L. Kunkel, and A.V. Andjelkovic Potential role of MCP-1 in endothelial cell tight junction 'opening': signaling via Rho and Rho kinase J. Cell Sci. 116 2003 4615 4628
54. S.M. Stamatovic, P. Shakui, R.F. Keep, B.B. Moore, S.L. Kunkel, N. Van Rooijen, and A.V. Andjelkovic Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability J. Cereb. Blood Flow Metab. 25 2005 593 606
55. J.J. Trout, H. Koenig, A.D. Goldstone, and C.Y. Lu Blood-brain barrier breakdown by cold injury. Polyamine signals mediate acute stimulation of endocytosis, vesicular transport, and microvillus formation in rat cerebral capillaries Lab. Invest. 55 1986 622 631
56. H. Wang, G. Zhang, Y. Wen, S. Yang, X. Xia, and Z.F. Fu Intracerebral administration of recombinant rabies virus expressing GM-CSF prevents the development of rabies after infection with street virus PLoS One 6 2011 e25414
57. Y. Wen, H. Wang, H. Wu, F. Yang, R.A. Tripp, R.J. Hogan, and Z.F. Fu Rabies virus expressing dendritic cell-activating molecules enhances the innate and adaptive immune response to vaccination J. Virol. 85 2011 1634 1644
58. WHO, 1992. WHO Expert Committee on rabies. In: World Health Organization Technical Report Series 824, pp. 1-84.
59. H. Wilde Failures of post-exposure rabies prophylaxis Vaccine 25 2007 7605 7609
60. R.E. Willoughby Jr., K.S. Tieves, G.M. Hoffman, N.S. Ghanayem, C.M. Amlie-Lefond, M.J. Schwabe, M.J. Chusid, and C.E. Rupprecht Survival after treatment of rabies with induction of coma N. Engl. J. Med. 352 2005 2508 2514
61. A. Yadav, V. Saini, and S. Arora MCP-1: chemoattractant with a role beyond immunity: a review Clin. Chim. Acta 411 2010 1570 1579
62. M.Z. Yousaf, M. Qasim, S. Zia, M. Khan, U.A. Ashfaq, and S. Khan Rabies molecular virology, diagnosis, prevention and treatment Virol. J. 9 2012 50
63. Y.J. Yu, Y. Zhang, M. Kenrick, K. Hoyte, W. Luk, Y. Lu, J. Atwal, J.M. Elliott, S. Prabhu, R.J. Watts, and M.S. Dennis Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target Sci. Transl. Med. 3 2011 84ra44
64. G. Zhang, and Z.F. Fu Complete genome sequence of a street rabies virus from Mexico J. Virol. 86 2012 10892 10893