Age-related changes of choroid plexus morphology, vascularization and epithelial proliferation

Authors

  • Golub D. Samardzija Department of Pathology, Faculty of Medicine, University of Novi Sad, Hajduk Veljkova 3, Novi Sad, Serbia
  • Bojana M. Andrejic-Visnjic Department of Histology and Embryology, Faculty of Medicine, University of Novi Sad, Hajduk Veljkova, Novi Sad, Serbia
  • Matilda A. Djolai Department of Histology and Embryology, Faculty of Medicine, University of Novi Sad, Hajduk Veljkova, Novi Sad, Serbia
  • Jelena R. Ilic-Sabo Department of Histology and Embryology, Faculty of Medicine, University of Novi Sad, Hajduk Veljkova, Novi Sad, Serbia
  • Jelena P. Amidzic Department of Histology and Embryology, Faculty of Medicine, University of Novi Sad, Hajduk Veljkova, Novi Sad, Serbia
  • Zoran Nikin Department of Pathology, Faculty of Medicine, University of Novi Sad, Hajduk Veljkova 3, Novi Sad, Serbia
  • Natali Z. Rakocevic Faculty of Medicine, University of Novi Sad, Hajduk Veljkova 3, Novi Sad, Serbia
  • Nikola N. Aleksic Faculty of Medicine, University of Novi Sad, Hajduk Veljkova 3, Novi Sad, Serbia
  • Borislav E. Dolamic Department for Specialistic-Consulting Work, Health Center Novi Sad, Bulevar cara Lazara 75, Novi Sad, Serbia
  • Biserka B. Vukomanovic-Djurdjevic Department of Histology, Military Medical Academy, University of Defence, Crnotravska 17, 11000 Belgrade, Serbia

DOI:

https://doi.org/10.2298/ABS201210014S

Keywords:

choroid plexus, ageing, psammoma body, amyloid, vascularization

Abstract

Paper description:

  • Dementia is thought to begin with changes in the blood-cerebrospinal fluid barrier, which makes ageing-associated alterations of the choroid plexus (ChP) a compelling topic.
  • This study provides a histomorphometric analysis of psammoma bodies (PBs), vasculature, amyloid deposition, and epithelium of the ChP among young, middle-aged and older individuals.
  • Ageing was associated with an increase in the number of PBs (specifically immature forms), and a significant decrease in the vascular area, accompanied by amyloid deposition.
  • Marked age-related changes provide a unique basis for comparison with pathological changes. Given the increase in immature PBs in the elderly, we challenge the given terminology.

Abstract: The choroid plexus (ChP) is essential for brain homeostasis by regulating the secretion of the cerebrospinal fluid (CSF). Despite a substantial body of work on the pathologically alterations of the ChP, there is lack of data concerning the naturally occurring morphological changes asso-ciated with ageing. In this study, we investigated 30 human ChP tissue samples that were divided into 3 groups according to age. Morphometric analysis of psammoma bodies (PBs) on hematoxylin and eosin (H&E)-stained samples and immunohistochemical analysis of ChP were performed (using antibodies to transmembrane phosphoglycoprotein protein CD34 and nuclear protein Ki-67). Amyloid deposits were detected using Congo red staining. Middle-aged and older individuals exhibited a significantly higher numerical density (ndPB) mostly as increased immature forms, which led us to question the proposed nomenclature. The proliferation rate of the ChP epithelium did not show significant difference between groups. The vascular area was markedly decreased and accompanied by amyloid deposition in blood vessel walls. While the deposits were limited to middle-sized blood vessels in the middle-aged group, in the older group deposits were also present around small vessels. The identified major morphological alterations of ageing ChP tissue provide further understanding of disfunctions of the blood-cerebrospinal fluid barrier that underlie neurodegenerative disorders.

Downloads

Download data is not yet available.

References

Ross MH, Pawlina W. Histology. 8th ed. Philadelphia: Lippincott Williams & Wilkins; 2018.

Lun MP, Monuki ES, Lehinen MK. Development and functions of the choroid plexus cerebrospinal fluid system. Nat Rev Neurosci. 2015;16(8):445-57. https://doi.org/10.1038/nrn3921

Spector R, Keep RF, Robert Snodgrass S, Smith QR, Johanson CE. A balanced view of choroid plexus structure and function: Focus on adult humans. Exp Neurol. 2015;267:78-86. https://doi.org/10.1016/j.expneurol.2015.02.032

Oreskovic D, Klarica M. The formation of cerebrospinal fluid: nearly a hundred years of interpretations and misinterpretations. Brain Res Rev. 2010;64(2):241-62. https://doi.org/10.1016/j.brainresrev.2010.04.006

Milhorat TH. Choroid plexus and cerebrospinal fluid production. Science. 1969;166(3912):1514-6. https://doi.org/10.1126/science.166.3912.1514

Milhorat TH. The third circulation revisited. J Neurosurg. 1975;42(6):628-45.

Milhorat TH. Structure and function of the choroid plexus and other sites of cerebrospinal fluid formation. Int Rev Cytol. 1976;47:225-88. https://doi.org/10.1016/s0074-7696(08)60090-x

Milhorat TH, Hammock MK, Fenstermacher JD, Rall DP, Levin VA. Cerebrospinal fluid production by the choroid plexus and brain. Science. 1971;173(3994):330-2. https://doi.org/10.1126/science.173.3994.330

Bulat M, Klarica M. Fluid filtration and reabsorption across microvascular walls: control by oncotic or osmotic pressure? Period. Biol. 2005;107(2):147-52.

Bulat M, Lupret V, Orešković D, Klarica M. Transventricular and transpial absorption of cerebrospinal fluid into cerebral microvessels. Coll Antropol. 2008;32(1):43-50.

Lipper S, Dalzell JC, Watkins PJ. Ultrastructure of psammoma bodies of meningioma in tissue culture. Arch Pathol Lab Med. 1979;103:670-5.

Živković VS, Stanojković MM, Antić MM. Psammoma bodies as signs of choroid plexus ageing-a morphometric analysis. Vojnosanit Pregl. 2017;74(11):1054-9. https://doi.org/10.2298/vsp160321205z

Jovanović I, Ugrenović S, Vasović Lj, Petrović D, Cekić S. Psammoma bodies - Friends or foes of the ageing choroid plexus. Med Hypotheses. 2010;74:1017-20. https://doi.org/10.1016/j.mehy.2010.01.006

Balusu S, Brkic M, Libert C, Vandenbroucke RE. The choroid plexus-cerebrospinal fluid interface in Alzheimer's disease: more than just a barrier. Neural Regen Res. 2016;11(4):534. https://doi.org/10.4103/1673-5374.180372

Brkic M, Balusu S, Van Wonterghem E, Gorlé N, Benilova I, Kremer A, et al. Amyloid β oligomers disrupt blood - CSF barrier integrity by activating matrix metalloproteinases. J Neurosci. 2015;35(37):12766-78. https://doi.org/10.1523/jneurosci.0006-15.2015

Redzic ZB, Preston JE, Duncan JA, Chodobski A, Szmydynger‐Chodobska J. The choroid plexus‐cerebrospinal fluid system: from development to aging. Curr Top Dev Biol. 2005;71:1-52. https://doi.org/10.1016/s0070-2153(05)71001-2

Bolos M, Antequera D, Aldudo J, Kristen H, Bullido MJ, Carro E. Choroid plexus implants rescue Alzheimer’s disease-like pathologies by modulating amyloid-β degradation. Cell Mol Life Sci. 2014;71(15):2947-55. https://doi.org/10.1007/s00018-013-1529-4

Serot JM, Foliguet B, Béné MC, Faure GC. Choroid plexus and ageing in rats: a morphometric and ultrastructural study. Eur J Neurosci. 2001;14(5):794-8. https://doi.org/10.1046/j.0953-816x.2001.01693.x

Chen RL, Kassem NA, Redzic ZB, Chen CP, Segal MB, Preston JE. Age-related changes in choroid plexus and blood-cerebrospinal fluid barrier function in the sheep. Exp Gerontol. 2009;44(4):289-96. https://doi.org/10.1016/j.exger.2008.12.004

Goal A: Better understand the biology of aging and its impact on the prevention, progression, and prognosis of disease and disability [Internet]. The National Institute on Aging; [cited 2021 Feb 14]. Available from: https://www.nia.nih.gov/about/aging-strategic-directions-research/goal-biology-impact

Naja S, Makhlouf MMED, Chehab MAH. An ageing world of the 21st century: a literature review. Int J Community Med Public Health. 2017;4:4363-9. https://doi.org/10.18203/2394-6040.ijcmph20175306

Jovanović I, Ugrenović S, Vasović L, Čukuranović R, Stoiljković N. Morphometric characteristics of choroid plexus epithelial cells in cases with significantly different psammoma bodies' presence. Microsc Res Tech. 2009;72(1):32-41. https://doi.org/10.1002/jemt.20642

Ageing and health. [Internet]. World Health Organization; [cited 2021 Feb 14]. Available from: https://www.who.int/news-room/fact-sheets/detail/ageing-and-health

Levine S. Choroid plexus: target for systematic disease and pathway to the brain. Lab Invest. 1987;56(3):231-3.

Moore GW, Laule C, Leung E, Pavlova V, Morgan BP, Esiri MM. Complement and humoral adaptive immunity in the human choroid plexus: roles for stromal concretions, basement membranes, and epithelium. J Neuropathol Exp. 2016;75(5):415-28. https://doi.org/10.1093/jnen/nlw017

Jovanović I, Ugrenović S, Vasović L, Stojanović I. Immunohistochemical and morphometric analysis of immunoglobulin light-chain immunoreactive amyloid in psammoma bodies of the human choroid plexus. Anat Sci Int. 2014;89(2):71-8. https://doi.org/10.1007/s12565-013-0201-2

Jovanović I, Stefanović N, Antić S, Ugrenović S, Djindjić B, Vidović N. Morphological and morphometric characteristics of choroid plexus psammoma bodies during the human aging. Ital J Anat Embryol. 2004;109(1):19-33. https://doi.org/10.1002/jemt.20442

Balusu S, Brkic M, Libert C, Vandenbroucke RE. The choroid plexus-cerebrospinal fluid interface in Alzheimer's disease: more than just a barrier. Neural Regen Res. 2016;11(4):534. https://doi.org/10.4103/1673-5374.180372

Serot JM, Béné MC, Faure GC. Choroid plexus, aging of the brain, and Alzheimer’s disease. Front Biosci. 2003;8(suppl):s515-21.

Vandenbroucke RE. A Hidden Epithelial Barrier in the Brain with a Central Role in Regulating Brain Homeostasis. Implications for Aging. Ann Am Thorac Soc. 2016;13Suppl5:S407-10. https://doi.org/10.1513/annalsats.201609-676aw

Damkier HH, Brown PD, Praetorius J. Cerebrospinal fluid secretion by the choroid plexus. Physiol Rev. 2013;93(4):1847-92. https://doi.org/10.1152/physrev.00004.2013

Kaur C, Rathnasamy G, Ling EA. The choroid plexus in healthy and diseased brain. J Neuropathol Exp Neurol. 2016; 75(3):198-213. https://doi.org/10.1093/jnen/nlv030

Das DK. Psammoma body: a product of dystrophic calcification or of biologically active process that aims at limiting the growth and spred of tumor? Diagn Cytoplathol. 2009;37(7):534-41. https://doi.org/10.1002/dc.21081

Jovanović I, Ugrenović S, Antić S, Stefanović N, Mihajlović D. Morphometric and some immunohistochemical characteristics of human choroids plexus stroma and psammoma bodies. Micros Res Tech. 2007;70(7):616-27. https://doi.org/10.1002/jemt.20442

Chen RL, Athauda SB, Kassem NA, Zhang Y, Segal MB, Preston JE. Decrease of transthyretin synthesis at the blood-cerebrospinal fluid barrier of old sheep. J Gerontol A Biol Sci Med Sci. 2005;60(7):852-8. https://doi.org/10.1093/gerona/60.7.852

Downloads

Published

2021-07-13

How to Cite

1.
Samardzija GD, Andrejic-Visnjic BM, Djolai MA, Ilic-Sabo JR, Amidzic JP, Nikin Z, Rakocevic NZ, Aleksic NN, Dolamic BE, Vukomanovic-Djurdjevic BB. Age-related changes of choroid plexus morphology, vascularization and epithelial proliferation. Arch Biol Sci [Internet]. 2021Jul.13 [cited 2024Dec.26];73(2):197-204. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/6043

Issue

Vol. 73 No. 2 (2021)

Section

Articles

License

Copyright (c) 2021 Archives of Biological Sciences

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.