Reduction of Microvessel Number and Length in the Cerebellum of Purkinje Cell Degeneration Mice

. 2024 Apr ; 23 (2) : 471-478. [epub] 20230418

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37071329

Grantová podpora
Cooperatio MED/DIAG Univerzita Karlova v Praze
CZ.02.1.01/0.0/0.0/16_019/0000787 (FIND) Ministerstvo Školství, Mládeže a Tělovýchovy

Odkazy

PubMed 37071329
DOI 10.1007/s12311-023-01556-y
PII: 10.1007/s12311-023-01556-y
Knihovny.cz E-zdroje

Degenerative effects of nerve tissues are often accompanied by changes in vascularization. In this regard, knowledge about hereditary cerebellar degeneration is limited. In this study, we compared the vascularity of the individual cerebellar components of 3-month-old wild-type mice (n = 8) and Purkinje cell degeneration (pcd) mutant mice, which represent a model of hereditary cerebellar degeneration (n = 8). Systematic random samples of tissue sections were processed, and laminin was immunostained to visualize microvessels. A computer-assisted stereology system was used to quantify microvessel parameters including total number, total length, and associated densities in cerebellar layers. Our results in pcd mice revealed a 45% (p < 0.01) reduction in the total volume of the cerebellum, a 28% (p < 0.05) reduction in the total number of vessels and a lower total length, approaching 50% (p < 0.001), compared to the control mice. In pcd mutants, cerebellar degeneration is accompanied by significant reduction in the microvascular network that is proportional to the cerebellar volume reduction therefore does not change density of in the cerebellar gray matter of pcd mice.

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Qu W, Johnson A, Kim JH, Lukowicz A, Svedberg D, Cvetanovic M. Inhibition of colony-stimulating factor 1 receptor early in disease ameliorates motor deficits in SCA1 mice. J Neuroinflamm. 2017;14:107. https://doi.org/10.1186/s12974-017-0880-z . DOI

Gyengesi E, Liang HZ, Millington C, Sonego S, Sirijovski D, Gunawardena D, et al. Investigation into the effects of tenilsetam on markers of neuroinflammation in GFAP-IL6 mice. Pharm Res. 2018;35:15. https://doi.org/10.1007/s11095-017-2326-9 . DOI

Wachter C, Eiden LE, Naumann N, Depboylu C, Weihe E. Loss of cerebellar neurons in the progression of lentiviral disease: effects of CNS-permeant antiretroviral therapy. J Neuroinflamm. 2016;13:13. https://doi.org/10.1186/s12974-016-0726-0 . DOI

Castrogiovanni P, Sanfilippo C, Imbesi R, Maugeri G, Lo Furno D, Tibullo D, et al. Brain CHID1 expression correlates with NRGN and CALB1 in healthy subjects and AD patients. Cells. 2021;10:18. https://doi.org/10.3390/cells10040882 . DOI

Patterson VL, Zullo AJ, Koenig C, Stoessel S, Jo H, Liu XR, et al. Neural-specific deletion of Htra2 causes cerebellar neurodegeneration and defective processing of mitochondrial OPA1. PLoS One. 2014;9:24. https://doi.org/10.1371/journal.pone.0115789 . DOI

Del Pilar C, Lebrón-Galán R, Pérez-Martín E, Pérez-Revuelta L, Ávila-Zarza CA, Alonso JR, et al. The selective loss of Purkinje cells induces specific peripheral immune alterations. Front Cell Neurosci. 2021;15:773696. https://doi.org/10.3389/fncel.2021.773696 . PubMed DOI PMC

Kolinko Y, Krakorova K, Cendelin J, Tonar Z, Kralickova M. Microcirculation of the brain: morphological assessment in degenerative diseases and restoration processes. Rev Neurosci. 2015;26:75–93. https://doi.org/10.1515/revneuro-2014-0049 . PubMed DOI

Skaaraas G, Melbye C, Puchades MA, Leung DSY, Jacobsen O, Rao SB, et al. Cerebral amyloid angiopathy in a mouse model of Alzheimer’s disease associates with upregulated angiopoietin and downregulated hypoxia-inducible factor. J Alzheimers Dis. 2021;83:1651–63. https://doi.org/10.3233/jad-210571 . PubMed DOI PMC

Fernandez-Klett F, Brandt L, Fernandez-Zapata C, Abuelnor B, Middeldorp J, Sluijs JA, et al. Denser brain capillary network with preserved pericytes in Alzheimer’s disease. Brain Pathol. 2020;30:1071–86. https://doi.org/10.1111/bpa.12897 . PubMed DOI PMC

Roitbak T, Li L, Cunningham LA. Neural stem/progenitor cells promote endothelial cell morphogenesis and protect endothelial cells against ischemia via HIF-1 alpha-regulated VEGF signaling. J Cereb Blood Flow Metab. 2008;28:1530–42. https://doi.org/10.1038/jcbfm.2008.38 . PubMed DOI

Mitoma H, Manto M, Gandini J. Recent advances in the treatment of cerebellar disorders. Brain Sci. 2019;10. https://doi.org/10.3390/brainsci10010011.

Cendelin J. From mice to men: lessons from mutant ataxic mice. Cerebellum Ataxias. 2014;1:4. https://doi.org/10.1186/2053-8871-1-4 . PubMed DOI PMC

Cendelin J, Cvetanovic M, Gandelman M, Hirai H, Orr HT, Pulst SM, et al. Consensus paper: strengths and weaknesses of animal models of spinocerebellar ataxias and their clinical implications. Cerebellum. 2022;21:452–81. https://doi.org/10.1007/s12311-021-01311-1 . PubMed DOI

Kolinko Y, Cendelin J, Kralickova M, Tonar Z. Smaller absolute quantities but greater relative densities of microvessels are associated with cerebellar degeneration in lurcher mice. Front Neuroanat. 2016;10:35. https://doi.org/10.3389/fnana.2016.00035 . PubMed DOI PMC

Babuska V, Houdek Z, Tuma J, Purkartova Z, Tumova J, Kralickova M, et al. Transplantation of embryonic cerebellar grafts improves gait parameters in ataxic lurcher mice. Cerebellum. 2015;14:632–41. https://doi.org/10.1007/s12311-015-0656-x . PubMed DOI

Cendelin J, Purkartova Z, Kubik J, Ulbricht E, Tichanek F, Kolinko Y. Long-term development of embryonic cerebellar grafts in two strains of lurcher mice. Cerebellum. 2018;17:428–37. https://doi.org/10.1007/s12311-018-0928-3 . PubMed DOI

Purkartova Z, Tichanek F, Kolinko Y, Cendelin J. Embryonic cerebellar graft morphology differs in two mouse models of cerebellar degeneration. Cerebellum. 2019;18:855–65. https://doi.org/10.1007/s12311-019-01067-9 . PubMed DOI

Fernandez-Gonzalez A, La Spada AR, Treadaway J, Higdon JC, Harris BS, Sidman RL, et al. Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science. 2002;295:1904–6. https://doi.org/10.1126/science.1068912 . PubMed DOI

Kyuhou S, Kato N, Gemba H. Emergence of endoplasmic reticulum stress and activated microglia in Purkinje cell degeneration mice. Neurosci Lett. 2006;396:91–6. https://doi.org/10.1016/j.neulet.2005.11.023 . PubMed DOI

Chakrabarti L, Eng J, Ivanov N, Garden GA, La Spada AR. Autophagy activation and enhanced mitophagy characterize the Purkinje cells of pcd mice prior to neuronal death. Mol Brain. 2009;2:24. https://doi.org/10.1186/1756-6606-2-24 . PubMed DOI PMC

Baltanas FC, Berciano MT, Valero J, Gomez C, Diaz D, Alonso JR, et al. Differential glial activation during the degeneration of Purkinje cells and mitral cells in the PCD mutant mice. Glia. 2013;61:254–72. https://doi.org/10.1002/glia.22431 . PubMed DOI

Mullen RJ, Eicher EM, Sidman RL. Purkinje cell degeneration, a new neurological mutation in the mouse. Proc Natl Acad Sci U S A. 1976;73:208–12. PubMed DOI PMC

Ghetti B, Norton J, Triarhou LC. Nerve cell atrophy and loss in the inferior olivary complex of “Purkinje cell degeneration” mutant mice. J Comp Neurol. 1987;260:409–22. https://doi.org/10.1002/cne.902600307 . PubMed DOI

Triarhou LC. Biological clues on neuronal degeneration based on theoretical fits of decay patterns: towards a mathematical neuropathology. Folia Neuropathol. 2010;48:3–10. PubMed

Triarhou LC, Norton J, Ghetti B. Anterograde transsynaptic degeneration in the deep cerebellar nuclei of Purkinje cell degeneration (pcd) mutant mice. Exp Brain Res. 1987;66:577–88. PubMed DOI

Blanks JC, Mullen RJ, LaVail MM. Retinal degeneration in the pcd cerebellar mutant mouse. II. Electron microscopic analysis. J Comp Neurol. 1982;212:231–46. https://doi.org/10.1002/cne.902120303 . PubMed DOI

LaVail MM, Blanks JC, Mullen RJ. Retinal degeneration in the pcd cerebellar mutant mouse .I. Light microscopic and autoradiographic analysis. J Comp Neurol. 1982;212:217–30. https://doi.org/10.1002/cne.902120302 . PubMed DOI

Blanks JC, Spee C. Retinal degeneration in the pcd/pcd mutant mouse: accumulation of spherules in the interphotoreceptor space. Exp Eye Res. 1992;54:637–44. PubMed DOI

O’Gorman S, Sidman RL. Degeneration of thalamic neurons in “Purkinje cell degeneration” mutant mice. I. Distribution of neuron loss. J Comp Neurol. 1985;234:277–97. https://doi.org/10.1002/cne.902340302 . PubMed DOI

Kolinko Y, Marsalova L, Pena SP, Kralickova M, Mouton PR. Stereological changes in microvascular parameters in hippocampus of a transgenic rat model of Alzheimer’s disease. J Alzheimers Dis. 2021;84:249–60. https://doi.org/10.3233/jad-210738 . PubMed DOI PMC

Kleiter N, Lametschwandtner A. Microvascularization of the cerebellum in the turtle, Pseudemys scripta elegans (Reptilia). A scanning electron microscope study of microvascular corrosion casts, including stereological measurements. Anat Embryol (Berl). 1995;191:145–53. PubMed DOI

Mouton PR. Principles and practices of unbiased stereology: an introduction for bioscientists. Baltimore, Maryland, USA: Johns Hopkins University Press; 2002.

Mouton PR. Unbiased stereology: a concise guide. Baltimore, Maryland, USA: Johns Hopkins University Press; 2011. DOI

Sterio DC. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc. 1984;134:127–36. https://doi.org/10.1111/j.1365-2818.1984.tb02501.x . PubMed DOI

Nyengaard JR, Marcussen N. The number of glomerular capillaries estimated by an unbiased and efficient stereological method. J Microsc. 1993;171:27–37. https://doi.org/10.1111/j.1365-2818.1993.tb03356.x . PubMed DOI

Lee GD, Aruna JH, Barrett PM, Lei DL, Ingram DK, Mouton PR. Stereological analysis of microvascular parameters in a double transgenic model of Alzheimer’s disease. Brain Res Bull. 2005;65:317–22. https://doi.org/10.1016/j.brainresbull.2004.11.024 . PubMed DOI

West MJ. Space balls revisited: stereological estimates of length with virtual isotropic surface probes. Front Neuroanat. 2018;12:49. https://doi.org/10.3389/fnana.2018.00049 . PubMed DOI PMC

Isaacs KR, Anderson BJ, Alcantara AA, Black JE, Greenough WT. Exercise and the brain: angiogenesis in the adult rat cerebellum after vigorous physical activity and motor skill learning. J Cereb Blood Flow Metab. 1992;12:110–9. https://doi.org/10.1038/jcbfm.1992.14 . PubMed DOI

Gundersen HJ, Jensen EB, Kieu K, Nielsen J. The efficiency of systematic sampling in stereology–reconsidered. J Microsc. 1999;193:199–211. PubMed DOI

Wang TY, Morgan JI. The Purkinje cell degeneration (pcd) mouse: an unexpected molecular link between neuronal degeneration and regeneration. Brain Res. 2007;1140:26–40. https://doi.org/10.1016/j.brainres.2006.07.065 . PubMed DOI

Rhyu IJ, Bytheway JA, Kohler SJ, Lange H, Lee KJ, Boklewski J, et al. Effects of aerobic exercise training on cognitive function and cortical vascularity in monkeys. Neuroscience. 2010;167:1239–48. https://doi.org/10.1016/j.neuroscience.2010.03.003 . PubMed DOI

Swain RA, Harris AB, Wiener EC, Dutka MV, Morris HD, Theien BE, et al. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience. 2003;117:1037–46. https://doi.org/10.1016/s0306-4522(02)00664-4 . PubMed DOI

Caddy KW, Biscoe TJ. Structural and quantitative studies on the normal C3H and Lurcher mutant mouse. Philos Trans R Soc Lond B Biol Sci. 1979;287:167–201. PubMed DOI

Vernet-der Garabedian B, Lemaigre-Dubreuil Y, Delhaye-Bouchaud N, Mariani J. Abnormal IL-1beta cytokine expression in the cerebellum of the ataxic mutant mice staggerer and lurcher. Brain Res Mol Brain Res. 1998;62:224–7. PubMed DOI

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