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Recording Leukocyte Rolling and Adhesion on Meningeal Vessels by Intravital Microscopy

  • Aline Silva de Miranda
  • Thiago Macedo Cordeiro
  • Milene Alvarenga Rachid
  • Antônio Lúcio Teixeira
Protocol
Part of the Neuromethods book series (NM, volume 142)

Abstract

Leukocyte infiltration in the central nervous system (CNS) has been implicated in several neuroinflammatory diseases, being an important step in the development of inflammatory response in the brain. The use of intravital microscopy technique allows direct in vivo assessment of leukocyte rolling and adhesion on cortical meningeal vessels. The current review highlights the use of intravital microscopy and its association with neuroinflammatory parameters in different models of experimental brain diseases such as HSV-1 encephalitis, dengue encephalitis, cerebral malaria, and hepatic encephalopathy. Herein, we also describe a detailed protocol of intravital microscopy of meningeal vessels, its advantages and major concerns.

Key words

Brain Pia mater vessels Intravital microscopy Leukocyte rolling Leukocyte adhesion Chemokines Mice 

Notes

Acknowledgments

The authors would like to thank FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais, Brazil), CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil), and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for financial support. ASM is a 2016 NARSAD Young Investigator Grant Awardee from the Brain and Behavior Research Foundation.

References

  1. 1.
    Engelhardt B (2006) Regulation of immune cell entry into the central nervous system. Results Probl Cell Differ 43:259–280CrossRefGoogle Scholar
  2. 2.
    Engelhardt B, Ransohoff RM (2005) The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol 26(9):485–495.  https://doi.org/10.1016/j.it.2005.07.004CrossRefPubMedGoogle Scholar
  3. 3.
    Ransohoff RM, Kivisakk P, Kidd G (2003) Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 3(7):569–581.  https://doi.org/10.1038/nri1130CrossRefPubMedGoogle Scholar
  4. 4.
    Alvarez JI, Teale JM (2007) Differential changes in junctional complex proteins suggest the ependymal lining as the main source of leukocyte infiltration into ventricles in murine neurocysticercosis. J Neuroimmunol 187(1–2):102–113.  https://doi.org/10.1016/j.jneuroim.2007.05.005CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Man S, Ubogu EE, Ransohoff RM (2007) Inflammatory cell migration into the central nervous system: a few new twists on an old tale. Brain Pathol 17(2):243–250.  https://doi.org/10.1111/j.1750-3639.2007.00067.xCrossRefPubMedGoogle Scholar
  6. 6.
    Greenwood J, Heasman SJ, Alvarez JI, Prat A, Lyck R, Engelhardt B (2011) Review: leucocyte-endothelial cell crosstalk at the blood-brain barrier: a prerequisite for successful immune cell entry to the brain. Neuropathol Appl Neurobiol 37(1):24–39.  https://doi.org/10.1111/j.1365-2990.2010.01140.xCrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Muller WA (2011) Mechanisms of leukocyte transendothelial migration. Annu Rev Pathol 6:323–344.  https://doi.org/10.1146/annurev-pathol-011110-130224CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Johnston B, Butcher EC (2002) Chemokines in rapid leukocyte adhesion triggering and migration. Semin Immunol 14(2):83–92.  https://doi.org/10.1006/smim.2001.0345CrossRefPubMedGoogle Scholar
  9. 9.
    Steiner O, Coisne C, Cecchelli R, Boscacci R, Deutsch U, Engelhardt B, Lyck R (2010) Differential roles for endothelial ICAM-1, ICAM-2, and VCAM-1 in shear-resistant T cell arrest, polarization, and directed crawling on blood-brain barrier endothelium. J Immunol 185(8):4846–4855.  https://doi.org/10.4049/jimmunol.0903732CrossRefPubMedGoogle Scholar
  10. 10.
    Engelhardt B, Wolburg H (2004) Mini-review: transendothelial migration of leukocytes: through the front door or around the side of the house? Eur J Immunol 34(11):2955–2963.  https://doi.org/10.1002/eji.200425327CrossRefPubMedGoogle Scholar
  11. 11.
    dos Santos AC, Barsante MM, Arantes RM, Bernard CC, Teixeira MM, Carvalho-Tavares J (2005) CCL2 and CCL5 mediate leukocyte adhesion in experimental autoimmune encephalomyelitis—an intravital microscopy study. J Neuroimmunol 162(1–2):122–129.  https://doi.org/10.1016/j.jneuroim.2005.01.020CrossRefPubMedGoogle Scholar
  12. 12.
    Handel TM, Johnson Z, Rodrigues DH, Dos Santos AC, Cirillo R, Muzio V, Riva S, Mack M, Deruaz M, Borlat F, Vitte PA, Wells TN, Teixeira MM, Proudfoot AE (2008) An engineered monomer of CCL2 has anti-inflammatory properties emphasizing the importance of oligomerization for chemokine activity in vivo. J Leukoc Biol 84(4):1101–1108.  https://doi.org/10.1189/jlb.0108061CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Rodrigues DH, Vilela MC, Barcelos LS, Pinho V, Teixeira MM, Teixeira AL (2010) Absence of PI3Kγ leads to increased leukocyte apoptosis and diminished severity of experimental autoimmune encephalomyelitis. J Neuroimmunol 222(1):90–94.  https://doi.org/10.1016/j.jneuroim.2010.02.016CrossRefPubMedGoogle Scholar
  14. 14.
    Rodrigues DH, Lacerda-Queiroz N, de Miranda AS, Fagundes CT, Campos RD, Arantes RE, Vilela Mde C, Rachid MA, Teixeira MM, Teixeira AL (2011) Absence of PAF receptor alters cellular infiltrate but not rolling and adhesion of leukocytes in experimental autoimmune encephalomyelitis. Brain Res 1385:298–306.  https://doi.org/10.1016/j.brainres.2011.02.036CrossRefPubMedGoogle Scholar
  15. 15.
    Vilela MC, Mansur DS, Lacerda-Queiroz N, Rodrigues DH, Arantes RME, Kroon EG, Campos MA, Teixeira MM, Teixeira AL (2008) Traffic of leukocytes in the central nervous system is associated with chemokine up-regulation in a severe model of herpes simplex encephalitis: an intravital microscopy study. Neurosci Lett 445(1):18–22.  https://doi.org/10.1016/j.neulet.2008.08.072CrossRefPubMedGoogle Scholar
  16. 16.
    Vilela MC, Mansur DS, Lacerda-Queiroz N, Rodrigues DH, Lima GK, Arantes RM, Kroon EG, da Silva Campos MA, Teixeira MM, Teixeira AL (2009) The chemokine CCL5 is essential for leukocyte recruitment in a model of severe Herpes simplex encephalitis. Ann N Y Acad Sci 1153:256–263.  https://doi.org/10.1111/j.1749-6632.2008.03959.xCrossRefPubMedGoogle Scholar
  17. 17.
    Vilela MC, Lima GK, Rodrigues DH, Lacerda-Queiroz N, Pedroso VSP, Miranda AS, Rachid MA, Kroon EG, Campos MA, Teixeira MM, Sellner J, Teixeira AL (2013) Absence of CCR5 increases neutrophil recruitment in severe herpetic encephalitis. BMC Neurosci 14:19–19.  https://doi.org/10.1186/1471-2202-14-19CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Vilela MC, Lima GK, Rodrigues DH, Lacerda-Queiroz N, Mansur DS, de Miranda AS, Rachid MA, Kroon EG, Vieira LQ, Campos MA, Teixeira MM, Teixeira AL (2010) TNFR1 plays a critical role in the control of severe HSV-1 encephalitis. Neurosci Lett 479(1):58–62.  https://doi.org/10.1016/j.neulet.2010.05.028CrossRefPubMedGoogle Scholar
  19. 19.
    Vilela MC, Lima GK, Rodrigues DH, Lacerda-Queiroz N, Pedroso VS, de Miranda AS, Rachid MA, Kroon EG, Campos MA, Teixeira MM, Teixeira AL (2016) Platelet activating factor (PAF) receptor deletion or antagonism attenuates severe HSV-1 meningoencephalitis. J Neuroimmune Pharmacol 11(4):613–621.  https://doi.org/10.1007/s11481-016-9684-7CrossRefPubMedGoogle Scholar
  20. 20.
    Amaral DC, Rachid MA, Vilela MC, Campos RD, Ferreira GP, Rodrigues DH, Lacerda-Queiroz N, Miranda AS, Costa VV, Campos MA, Kroon EG, Teixeira MM, Teixeira AL (2011) Intracerebral infection with dengue-3 virus induces meningoencephalitis and behavioral changes that precede lethality in mice. J Neuroinflammation 8:23.  https://doi.org/10.1186/1742-2094-8-23CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Lacerda-Queiroz N, Rodrigues DH, Vilela MC, Miranda AS, Amaral DC, Camargos ER, Carvalho LJ, Howe CL, Teixeira MM, Teixeira AL (2010) Inflammatory changes in the central nervous system are associated with behavioral impairment in Plasmodium berghei (strain ANKA)-infected mice. Exp Parasitol 125(3):271–278.  https://doi.org/10.1016/j.exppara.2010.02.002CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Lacerda-Queiroz N, Rodrigues DH, Vilela MC, Rachid MA, Soriani FM, Sousa LP, Campos RD, Quesniaux VF, Teixeira MM, Teixeira AL (2012) Platelet-activating factor receptor is essential for the development of experimental cerebral malaria. Am J Pathol 180(1):246–255.  https://doi.org/10.1016/j.ajpath.2011.09.038CrossRefPubMedGoogle Scholar
  23. 23.
    Lacerda-Queiroz N, Lima OC, Carneiro CM, Vilela MC, Teixeira AL, Teixeira-Carvalho A, Araujo MS, Martins-Filho OA, Braga EM, Carvalho-Tavares J (2011) Plasmodium berghei NK65 induces cerebral leukocyte recruitment in vivo: an intravital microscopic study. Acta Trop 120(1–2):31–39.  https://doi.org/10.1016/j.actatropica.2011.04.020CrossRefPubMedGoogle Scholar
  24. 24.
    Faleiros BE, Miranda AS, Campos AC, Gomides LF, Kangussu LM, Guatimosim C, Camargos ERS, Menezes GB, Rachid MA, Teixeira AL (2014) Up-regulation of brain cytokines and chemokines mediates neurotoxicity in early acute liver failure by a mechanism independent of microglial activation. Brain Res 1578(Supplement C):49–59.  https://doi.org/10.1016/j.brainres.2014.07.001CrossRefPubMedGoogle Scholar
  25. 25.
    Teixeira MM, Vilela MC, Soriani FM, Rodrigues DH, Teixeira AL (2010) Using intravital microscopy to study the role of chemokines during infection and inflammation in the central nervous system. J Neuroimmunol 224(1–2):62–65.  https://doi.org/10.1016/j.jneuroim.2010.05.018CrossRefPubMedGoogle Scholar
  26. 26.
    Prunier C, Chen N, Ritsma L, Vrisekoop N (2017) Procedures and applications of long-term intravital microscopy. Methods 128:52–64.  https://doi.org/10.1016/j.ymeth.2017.06.029CrossRefPubMedGoogle Scholar
  27. 27.
    Cabrales P, Carvalho LJ (2010) Intravital microscopy of the mouse brain microcirculation using a closed cranial window. J Vis Exp (45).  https://doi.org/10.3791/2184
  28. 28.
    Holtmaat A, Bonhoeffer T, Chow DK, Chuckowree J, De Paola V, Hofer SB, Hubener M, Keck T, Knott G, Lee WC, Mostany R, Mrsic-Flogel TD, Nedivi E, Portera-Cailliau C, Svoboda K, Trachtenberg JT, Wilbrecht L (2009) Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat Protoc 4(8):1128–1144.  https://doi.org/10.1038/nprot.2009.89CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Mostany R, Portera-Cailliau C (2008) A craniotomy surgery procedure for chronic brain imaging. J Vis Exp 12:680.  https://doi.org/10.3791/680CrossRefGoogle Scholar
  30. 30.
    Zuluaga-Ramirez V, Rom S, Persidsky Y (2015) Craniula: a cranial window technique for prolonged imaging of brain surface vasculature with simultaneous adjacent intracerebral injection. Fluids Barriers CNS 12:24.  https://doi.org/10.1186/s12987-015-0021-yCrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Aline Silva de Miranda
    • 1
    • 2
  • Thiago Macedo Cordeiro
    • 1
  • Milene Alvarenga Rachid
    • 3
  • Antônio Lúcio Teixeira
    • 1
    • 4
  1. 1.Laboratório Interdisciplinar de Investigação Médica, Faculdade de MedicinaUniversidade Federal de Minas GeraisBelo HorizonteBrasil
  2. 2.Laboratório de Neurobiologia, Departamento de MorfologiaInstituto de Ciências Biológicas, Universidade Federal de Minas GeraisBelo HorizonteBrasil
  3. 3.Departamento de Patologia GeralUniversidade Federal de Minas GeraisBelo HorizonteBrasil
  4. 4.Neuropsychiatry Program, Department of Psychiatry & Behavioral SciencesMcGovern Medical School, University of Texas Health Science Center at HoustonHoustonUSA

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