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Naizaque G., J. R. ., & Torres-Fernández., O. . (2016). Immunoreactivity to calbindin in purkinje cells in the cerebellum of mice is not affected by rabies virus infection. Biosalud, 15(2), 9–19. https://doi.org/10.17151/biosa.2016.15.2.2
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Abstract
Introduction: Calbindin (CB) is a regulatory protein of intracellular calcium, and the cerebellar Purkinje cell is the neuron with the highest concentration of CB. Loss of CB immunoreactivity has been demonstrated in different areas of the nervous system in rabies virus-infected mice, but the study of this phenomena in the cerebellum lacked. Objective: To determine the effect of inoculation with rabies virus on the expression of CB in Purkinje cells of the cerebellum of mice. Methodology: Mice were intramuscularly inoculated with rabies virus. Animals were sacrificed when they reached an advanced stage of the disease and then they were fixed by intracardiac perfusion with 4% paraformaldehyde. Cerebellums were extracted and sagittal sections 50 microns thick were obtained in a vibratome. These were processed by immunohistochemistry to reveal the presence of CB protein or rabies virus antigens. The same procedure was performed with uninfected animals (controls). Results: Purkinje cells were massively infected with rabies virus. In the microscopic panoramic images observed was found that only these cells are immunoreactive to CB. No significant difference in CB immunoreactivity evaluated by optical densitometry was found between infected animals and controls. Conclusion: The expression of CB in Purkinje cells of the cerebellum appears not to be affected by infection with rabies unlike what has been shown in other areas of the mouse nervous system.
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References
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13. Leuba G, Kraftsik R, Saini K. Quantitative distribution of parvalbumin, calretinin, and calbindin D-28k immunoreactive neurons in the visual cortex of normal and Alzheimer cases. Exp Neurol 1998; 152:278–91.
14. Ahmadian SS, Rezvanian A, Peterson M, Weintraub S, Bigio EH, Mesulam MM, Geula C. Loss of calbindin-D28K is associated with the full range of tangle pathology within basal forebrain cholinergic neurons in Alzheimer’s disease. Neurobiol aging 2015; 36:3163-70.
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17. Masliah E, Ge N, Achim CL, Wiley CA. Differential vulnerability of calbindin-immunoreactive neurons in HIV encephalitis. J. Neuropathol Exp Neurol 1995; 54:350-7.
18. Schmidt H. Three functional facets of calbindin D-28k. Front Mol Neurosci 2012; 5:25. doi: 10.3389/fnmol.2012.00025.
19. Schwaller B. The continuing disappearance of “pure” Ca2+ buffers. Cell Mol Life Sci 2009; 66:275–300.
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21. Torres-Fernández O, Yepes GE, Gómez JE, Pimienta HJ. Calbindin distribution in cortical and subcortical brain structures of normal and rabies-infected mice. Int J Neurosci 2005;
115:1375–82.
22. Ladogana A, Bouzamondo E, Pocchiari M, Tsiang H. Modification of tritiated γ-amino-n-butyric acid transport in rabies virus-infected primary cortical cultures. J Gen Virol 1994; 75:623–7.
23. Rengifo AC, Torres-Fernández O. Disminución del número de neuronas que expresan GABA en la corteza cerebral de ratones infectados con rabia. Biomédica 2007; 27:548–58.
24. Lamprea N, Torres-Fernández O. Evaluación inmunohistoquímica de la expresión de calbindina en el cerebro de ratones en diferentes tiempos después de la inoculación con el virus de la rabia. Colomb Med 2008; 39 (Supl.3): 7–13.
25. Monroy-Gómez J, Torres-Fernández O. Distribución de calbindina y parvoalbúmina y efecto del virus de la rabia sobre su expresión en la médula espinal de ratones. Biomédica 2013; 33:564–73.
26. Vigot R, Kado RT, Batini C. Increased calbindin-D28K immunoreactivity in rat cerebellar Purkinje cell with excitatory amino acids agonists is not dependent on protein synthesis. Arch Ital Biol 2004; 142:69–75.
27. Koprowski H. The mouse inoculation test. En: Meslin FX, Kaplan MM, Koprowski H, editores. Laboratory Techniques in Rabies. Geneva: World Health Organization, 4th ed; 1996. p. 80–7.
28. Lamprea NP, Ortega LM, Santamaría G, Sarmiento L, Torres-Fernández O. Elaboración y evaluación de un antisuero para la detección inmunohistoquímica del virus de la rabia en tejido cerebral fijado en aldehídos. Biomédica 2010; 30:146-51.
29. Paxinos G, Franklyn, KB. The mouse brain in stereotaxic coordinates. San Diego: Academic Press; 2001.
30. Torres-Fernández O, Santamaría G, Monroy-Gómez J. Dinámica neuroanatómica de infección celular en la ruta de dispersión del virus de la rabia en ratones inoculados por vía intramuscular. Biomédica 2015; 35 (Supl. 3):113-4.
31. Jackson AC, Rossiter JP. Apoptosis plays an important role in experimental rabies virus infection. J Virol 1997; 71:5603-07.
32. Jackson AC, Park H. Apoptotic cell death in experimental rabies in suckling mice. Acta Neuropathol 1998; 95:159-64.
33. Johnson R. Selective vulnerability of neural cells to viral infection. Brain 1980; 103:447-72.
34. Schwaller B, Meyer M, Schiffmann S. ‘New’ functions for ‘old’ proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 2002; 1:241–58
35. Krebs J, Heizmann CW. Calcium-binding proteins and EF-hand principle. En: Krebs J, Michalak M, editores. Calcium: A matter of life or death. Amsterdam: Elsevier B.V.; 2007. p. 51-93.
36. Rengifo AC, Torres-Fernández O. Cambios en los sistemas de neurotransmisión excitador e inhibitorio en el cerebelo de ratones infectados con virus de la rabia. Biomédica 2013; 33 (Supl. 2):80-81.
37. Winsky L, Kuźnicki J. Antibody recognition of calcium-binding proteins depends on their calciumbinding status. J Neurochem 1996; 66:764–71.
38. Verdes JM, de Sant’Ana FJ, Sabalsagaray MJ, Okada K, Calliari A, Moraña JA, de Barros CS. Calbindin D28k distribution in neurons and reactive gliosis in cerebellar cortex of natural rabies virus-infected cattle. J Vet Diagn Invest 2016. May 6. doi: 10.1177/1040638716644485.
39. Hof P, Glezer I, Condé F, Flagg R, Rubin M, Nimchinsky E, Vogt DM. Cellular distribution of the calciumbinding proteins parvalbumin, calbindin and calretinin in the neocortex of ammals: phylogenetic and developmental patterns. J Chem Neuroanat 1999; 16:77-116
40. Rockel A, Hiorns R, Powell T. The basic uniformity in structure of the neocortex. Brain 1980; 103: 221-44.
2. Fooks AR, Banyard AC, Horton DL, Johnson N, McElhinney LM, Jackson AC. Current status of rabies and prospects for elimination. Lancet 2014; 384:1389–99.
3. Vigilato M, Cosivi O, Clavijo A, Silva H. Rabies update for Latin America and the Caribbean. Emerg Infect Dis 2013; 19:678-9.
4. Cediel N, de la Hoz F, Villamil LC, Romero J, Díaz A. Epidemiología de la rabia canina en Colombia. Rev Salud Pública 2010; 12: 368–79.
5. Jackson AC. Rabies. Neurol Clin 2008; 26:717–26.
6. Hemachudha T, Ugolini G, Wacharapluesadee S, Sungkarat W, Shuangshoti S, Laothamatas J. Human rabies: neuropathogenesis, diagnosis, and management. Lancet Neurol 2013; 12:498–513.
7. Iwasaki Y, Tobita M. Pathology. En: Jackson AC, Wunner WH, editores. Rabies. San Diego: Academic Press 2002. p. 283-306.
8. Jackson AC, Randle E, Lawrance G, Rossiter JP. Neuronal apoptosis does not play an important role in human rabies encephalitis. J Neurovirol 2008; 14:368–75.
9. Suja MS, Mahadevan A, Madhusudana SN, Shankar SK. Role of apoptosis in rabies viral encephalitis: A comparative study in mice, canine, and human brain with a review of literature. Patholog Res Int 2011; 2011:374286. doi: 10.4061/2011/374286.
10. Fu ZF, Jackson AC. Neuronal dysfunction and death in rabies virus infection. J Neurovirol 2005; 11:101–6.
11. Torres-Fernández O, Yepes G, Gómez J, Pimienta H. Efecto de la infección por el virus de la rabia sobre la expresión de parvoalbúmina, calbindina y calretinina en la corteza cerebral de ratones. Biomédica 2004; 24:63-78.
12. Andressen C, Blumcke I, Celio M. Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 1993; 271:181-208.
13. Leuba G, Kraftsik R, Saini K. Quantitative distribution of parvalbumin, calretinin, and calbindin D-28k immunoreactive neurons in the visual cortex of normal and Alzheimer cases. Exp Neurol 1998; 152:278–91.
14. Ahmadian SS, Rezvanian A, Peterson M, Weintraub S, Bigio EH, Mesulam MM, Geula C. Loss of calbindin-D28K is associated with the full range of tangle pathology within basal forebrain cholinergic neurons in Alzheimer’s disease. Neurobiol aging 2015; 36:3163-70.
15. Iacopino AM, Christakos S. Specific reduction of calcium-binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc Natl Acad Sci U S A 1990; 87:4078–82.
16. Beasley C, Zhang Z, Patten I, Reynolds G. Selective deficits in prefrontal cortical GABAergic neurons in schizophrenia defined by the presence of calcium binding proteins. Biol Psychiatry.2002; 52:708- 15.
17. Masliah E, Ge N, Achim CL, Wiley CA. Differential vulnerability of calbindin-immunoreactive neurons in HIV encephalitis. J. Neuropathol Exp Neurol 1995; 54:350-7.
18. Schmidt H. Three functional facets of calbindin D-28k. Front Mol Neurosci 2012; 5:25. doi: 10.3389/fnmol.2012.00025.
19. Schwaller B. The continuing disappearance of “pure” Ca2+ buffers. Cell Mol Life Sci 2009; 66:275–300.
20. Flace P, Lorusso L, Laiso G, Rizzi A, Cagiano R, Nico B, et al. Calbindin-D28K immunoreactivity in the human cerebellar cortex. Anat Rec 2014; 297:1306–15.
21. Torres-Fernández O, Yepes GE, Gómez JE, Pimienta HJ. Calbindin distribution in cortical and subcortical brain structures of normal and rabies-infected mice. Int J Neurosci 2005;
115:1375–82.
22. Ladogana A, Bouzamondo E, Pocchiari M, Tsiang H. Modification of tritiated γ-amino-n-butyric acid transport in rabies virus-infected primary cortical cultures. J Gen Virol 1994; 75:623–7.
23. Rengifo AC, Torres-Fernández O. Disminución del número de neuronas que expresan GABA en la corteza cerebral de ratones infectados con rabia. Biomédica 2007; 27:548–58.
24. Lamprea N, Torres-Fernández O. Evaluación inmunohistoquímica de la expresión de calbindina en el cerebro de ratones en diferentes tiempos después de la inoculación con el virus de la rabia. Colomb Med 2008; 39 (Supl.3): 7–13.
25. Monroy-Gómez J, Torres-Fernández O. Distribución de calbindina y parvoalbúmina y efecto del virus de la rabia sobre su expresión en la médula espinal de ratones. Biomédica 2013; 33:564–73.
26. Vigot R, Kado RT, Batini C. Increased calbindin-D28K immunoreactivity in rat cerebellar Purkinje cell with excitatory amino acids agonists is not dependent on protein synthesis. Arch Ital Biol 2004; 142:69–75.
27. Koprowski H. The mouse inoculation test. En: Meslin FX, Kaplan MM, Koprowski H, editores. Laboratory Techniques in Rabies. Geneva: World Health Organization, 4th ed; 1996. p. 80–7.
28. Lamprea NP, Ortega LM, Santamaría G, Sarmiento L, Torres-Fernández O. Elaboración y evaluación de un antisuero para la detección inmunohistoquímica del virus de la rabia en tejido cerebral fijado en aldehídos. Biomédica 2010; 30:146-51.
29. Paxinos G, Franklyn, KB. The mouse brain in stereotaxic coordinates. San Diego: Academic Press; 2001.
30. Torres-Fernández O, Santamaría G, Monroy-Gómez J. Dinámica neuroanatómica de infección celular en la ruta de dispersión del virus de la rabia en ratones inoculados por vía intramuscular. Biomédica 2015; 35 (Supl. 3):113-4.
31. Jackson AC, Rossiter JP. Apoptosis plays an important role in experimental rabies virus infection. J Virol 1997; 71:5603-07.
32. Jackson AC, Park H. Apoptotic cell death in experimental rabies in suckling mice. Acta Neuropathol 1998; 95:159-64.
33. Johnson R. Selective vulnerability of neural cells to viral infection. Brain 1980; 103:447-72.
34. Schwaller B, Meyer M, Schiffmann S. ‘New’ functions for ‘old’ proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 2002; 1:241–58
35. Krebs J, Heizmann CW. Calcium-binding proteins and EF-hand principle. En: Krebs J, Michalak M, editores. Calcium: A matter of life or death. Amsterdam: Elsevier B.V.; 2007. p. 51-93.
36. Rengifo AC, Torres-Fernández O. Cambios en los sistemas de neurotransmisión excitador e inhibitorio en el cerebelo de ratones infectados con virus de la rabia. Biomédica 2013; 33 (Supl. 2):80-81.
37. Winsky L, Kuźnicki J. Antibody recognition of calcium-binding proteins depends on their calciumbinding status. J Neurochem 1996; 66:764–71.
38. Verdes JM, de Sant’Ana FJ, Sabalsagaray MJ, Okada K, Calliari A, Moraña JA, de Barros CS. Calbindin D28k distribution in neurons and reactive gliosis in cerebellar cortex of natural rabies virus-infected cattle. J Vet Diagn Invest 2016. May 6. doi: 10.1177/1040638716644485.
39. Hof P, Glezer I, Condé F, Flagg R, Rubin M, Nimchinsky E, Vogt DM. Cellular distribution of the calciumbinding proteins parvalbumin, calbindin and calretinin in the neocortex of ammals: phylogenetic and developmental patterns. J Chem Neuroanat 1999; 16:77-116
40. Rockel A, Hiorns R, Powell T. The basic uniformity in structure of the neocortex. Brain 1980; 103: 221-44.
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