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Identification of Key Molecular Biomarkers Involved in Reactive And Ojeda‑Pérez et al. Fluids Barriers CNS (2021) 18:30 https://doi.org/10.1186/s12987‑021‑00263‑2 Fluids and Barriers of the CNS RESEARCH Open Access Identifcation of key molecular biomarkers involved in reactive and neurodegenerative processes present in inherited congenital hydrocephalus Betsaida Ojeda‑Pérez1,2, José A. Campos‑Sandoval3, María García‑Bonilla1,2, Casimiro Cárdenas‑García3, Patricia Páez‑González1,2*† and Antonio J. Jiménez1,2*† Abstract Background: Periventricular extracellular oedema, myelin damage, infammation, and glial reactions are common neuropathological events that occur in the brain in congenital hydrocephalus. The periventricular white matter is the most afected region. The present study aimed to identify altered molecular and cellular biomarkers in the neocortex that can function as potential therapeutic targets to both treat and evaluate recovery from these neurodegenerative conditions. The hyh mouse model of hereditary hydrocephalus was used for this purpose. Methods: The hyh mouse model of hereditary hydrocephalus (hydrocephalus with hop gait) and control littermates without hydrocephalus were used in the present work. In tissue sections, the ionic content was investigated using energy dispersive X‑ray spectroscopy scanning electron microscopy (EDS‑SEM). For the lipid analysis, matrix‑assisted laser desorption ionization mass spectrometry imaging (MALDI‑MSI) was performed in frozen sections. The expression of proteins in the cerebral white matter was analysed by mass spectrometry. The oligodendrocyte progenitor cells (OPCs) were studied with immunofuorescence in cerebral sections and whole‑mount preparations of the ventricle walls. Results: High sodium and chloride concentrations were found indicating oedema conditions in both the periven‑ tricular white matter and extending towards the grey matter. Lipid analysis revealed lower levels of two phosphati‑ dylinositol molecular species in the grey matter, indicating that neural functions were altered in the hydrocephalic mice. In addition, the expression of proteins in the cerebral white matter revealed evident deregulation of the pro‑ cesses of oligodendrocyte diferentiation and myelination. Because of the changes in oligodendrocyte diferentiation in the white matter, OPCs were also studied. In hydrocephalic mice, OPCs were found to be reactive, overexpressing the NG2 antigen but not giving rise to an increase in mature oligodendrocytes. The higher levels of the NG2 antigen, diacylglycerophosphoserine and possibly transthyretin in the cerebrum of hydrocephalic hyh mice could indicate cell reactions that may have been triggered by infammation, neurocytotoxic conditions, and ischaemia. *Correspondence: [email protected]; [email protected] †Patricia Páez‑González and Antonio J Jiménez contributed equally to this work 1 Department of Cell Biology, Genetics, and Physiology, Facultad de Ciencias, Universidad de Málaga, Campus de Teatinos, 29071 Malaga, Spain Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ojeda‑Pérez et al. Fluids Barriers CNS (2021) 18:30 Page 2 of 29 Conclusion: Our results identify possible biomarkers of hydrocephalus in the cerebral grey and white matter. In the white matter, OPCs could be reacting to acquire a neuroprotective role or as a delay in the oligodendrocyte maturation. Keywords: Biomarkers, Hereditary hydrocephalus, Energy dispersive X‑ray spectroscopy (EDS), Lipids, Ultrahigh‑ performance liquid chromatography‑high‑resolution mass spectrometry (UHPLC–HRMS), Matrix‑assisted laser desorption ionization mass spectrometry imaging (MALDI‑MSI), NG2 antigen, Oligodendrocyte progenitor cells, Proteomic Introduction Te presence of oedema conditions in the cerebrum, In hereditary congenital obstructive hydrocephalus, the both in the periventricular white matter and deeper in elevation of intracranial pressure and enlargement of the grey matter, was revealed. Additionally, the expres- the cerebral ventricles induce injury in the brain paren- sion of lipids and proteins was investigated by matrix- chyma [1]. Consequently, there is a gradual stretching assisted laser desorption ionization mass spectrometry and destruction of periventricular white matter axons imaging (MALDI-MSI) and ultrahigh-performance liq- and a delay in their myelination [2]. Ten, as in other uid chromatography-high-resolution mass spectrometry pathological events, such as stroke or brain injury, axonal (UHPLC–HRMS), respectively. Te results suggested a damage is considered the main pathological change [3– combination of neurodegenerative processes. Analysis 5]. Te external capsule and corpus callosum have been of proteins in the white matter revealed deregulation of described as the most susceptible white matter structures oligodendrocyte diferentiation and myelination. For this to sufer damage in hydrocephalus [4, 6–9]. Additionally, reason, oligodendrocyte progenitor cells (OPCs) were in congenital hydrocephalus, astrocyte and microglial cell also studied, and they were found to be reactive, but they activation is a common pathological event that can afect did not appear to give rise to a higher density of mature the cerebral white matter [9–17]. Activated microglia has oligodendrocytes. Our results in the neurodegenerative been implicated in the destruction of the white matter in conditions studied in the brain parenchyma: i) suggest a the early phases of hydrocephalus [17, 18]. Other harmful delayed OPC diferentiation and ii) show overexpression conditions afecting the periventricular walls in congeni- of neuron/glial NG2 antigen in the reactive OPCs that tal hydrocephalus need to be considered such as the pres- could play a neuroprotective role [29]. ence of periventricular oedema, which is refected by the levels of osmolytes [19], and high levels of the proinfam- Material and methods matory cytokine TNFα and neuroexcitotoxic glutamate Experimental animals [19, 20]. Twenty-day-old mutant hydrocephalic hyh mice (hydro- In the present study, we looked for biomarkers of cephalus with hop gait, B6C3Fe- a/a-hyh/J strain) were molecular and cellular responses under detrimental con- used as a model of congenital obstructive hydrocephalus, ditions that may also function as potential therapeutic and their non-hydrocephalic wild-type (wt) littermates targets. Te hyh mouse model of hereditary congenital were used as controls. Te hyh mice were originally hydrocephalus [21] was used for this purpose. Te origin obtained from Te Jackson Laboratory (Bar Harbor, and histopathology of hydrocephalus in the hyh mouse ME, USA). Tey were bred by the Animal Experimen- share similarities with that of hydrocephalus cases in tation Service of the University of Malaga on a 12:12 h humans [20, 22–24]. Te hyh mouse presents a muta- light/dark cycle at 22 °C and provided standard food and tion in the Napa gene, which encodes N-ethylmaleimide- water ad libitum. Wt and mutant hyh mice with severe sensitive factor attachment protein alpha (α-Snap), which hydrocephalus were identifed by clinical inspection afects membrane trafcking and possibly cell adhesion and genotyping [30]. Te experimental procedures were in the neuroepithelium during development [24, 25]. approved by the Institutional Animal Care and Use Com- As a consequence, the hyh mouse develops obstructive mittee of the University of Malaga (CEUMA). Tus, the hydrocephalus with severe damage to the neocortex [17, experiments were designed and the animals were housed, 26–28]. handled, cared for and processed in accordance with Te present study was focused on key pathophysi- European and Spanish laws (RD53/2013 and 2010/63UE) ological events in hydrocephalus. First, the ionic envi- and following the ARRIVE guidelines [31]. For EDS-SEM, ronment was examined through an analysis of the MALDI-MSI, and UHPLC–HRMS, the animals were elemental spectrum using scanning electron microscopy sacrifced by cervical dislocation. Ten, the brains were by energy dispersive X-ray spectroscopy (SEM–EDS). quickly dissected under cold conditions, frozen in dry ice, Ojeda‑Pérez et al. Fluids Barriers CNS (2021) 18:30 Page 3 of 29 and stored at − 80 °C. Te procedure between dissection (v:v:v) ACN:H20:TFA and sprayed over the tissue samples and freezing took less than fve minutes. Te mice were using the SunCollect device (SunChrom, Friedrichsdorf, also anaesthetized with Dolethal (sodium pentobarbital; Germany). Te spray settings were as follows: spray-head
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