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Oligodendrocyte and Myelin neuroglia Article Ultrastructural Remodeling of the Neurovascular Unit in the Female Diabetic db/db Model—Part III: Oligodendrocyte and Myelin Melvin R. Hayden 1,2,*, Deana G. Grant 3, Aranyra Aroor 1,2,4 and Vincent G. DeMarco 1,2,4,5 1 Diabetes and Cardiovascular Center, University of Missouri School of Medicine, Columbia, MO 65212, USA; [email protected] (A.A.); [email protected] (V.G.D.) 2 Division of Endocrinology and Metabolism, Department of Medicine, University of Missouri, Columbia, MO 63212, USA 3 Electron Microscopy Core Facility, University of Missouri, Columbia, MO 65211, USA; [email protected] 4 Research Service, Harry S. Truman Memorial Veterans Hospital, Columbia, MO 65212, USA 5 Department of Medical Pharmacology and Physiology, University of Missouri, Columbia, MO 65212, USA * Correspondence: [email protected]; Tel.: +1-573-346-3019 Received: 9 October 2018; Accepted: 5 November 2018; Published: 8 November 2018 Abstract: Obesity, insulin resistance, and type 2 diabetes mellitus are associated with diabetic cognopathy. In this study, we tested the hypothesis that neurovascular unit(s) (NVU), oligodendrocytes, and myelin within cerebral cortical grey matter and deeper transitional zone regions between the cortical grey matter and white matter may be abnormal. The monogenic (Leprdb) female diabetic db/db [BKS.CgDock7m +/+ Leprdb/J] (DBC) mouse model was utilized for this ultrastructural study. Upon sacrifice (20 weeks of age), left-brain hemispheres of the DBC and age-matched non-diabetic wild type control C57BL/KsJ (CKC) mice were immediately immersion-fixed. We found prominent remodeling of oligodendrocytes with increased nuclear chromatin condensation and volume and increased numbers of active myelination sites of the cytoplasm in transition zones. Marked dysmyelination with outer myelin lamellae sheath splitting, separation, and ballooning with aberrant mitochondria in grey matter and similar myelin remodeling changes with marked disarray with additional axonal collapse in transitional zones in DBC as compared to CKC models. Keywords: db/db mouse model; myelin; neurovascular unit; oligodendrocyte; subcortical white matter; type 2 diabetes 1. Introduction Myelin is a multilayered lamellar sheath that enwraps axons in the grey and white matter in the brain and is synthesized in the brain by the oligodendroglia. The myelin sheath provides axonal protection and allows the saltatory conduction of the action potential. Oligodendrocytes (OLs), oligodendrocyte precursor cells (OPC), and oligodendrocyte lineage cells are specialized glial cells responsible for the synthesis, wrapping ensheathment, and compacting of myelin in myelinated axons [1–3]. Rudolf Ludwig Virchow (1821–1902) introduced the term myelin and defined it as medullary matter (Markstoff), or myeline, that in extremely large quantity fills up the interval between the axon axis-cylinder and the sheath in primitive nerve-fibers [4]. Michalski and Kothary [1] have set forth a paradigm for development of mature OLs in four distinct phases: (i) the birth, migration and proliferation of OPCs, that occurs in waves; followed by (ii) morphological differentiation with the OL establishing an expansive synthetic Neuroglia 2018, 1, 351–364; doi:10.3390/neuroglia1020024 www.mdpi.com/journal/neuroglia Neuroglia 2018, 1 352 network of OL cytoplasmic processes; followed by (iii) axonal contact, which leads to myelin wrapping—ensheathment of targeted neuronal axons with ensuing generation of extremely electron Neuroglia 2018, 1, x FOR PEER REVIEW 2 of 14 dense and compact myelin with an enduring (iv) long-term trophic and metabolic support system for maintenancecytoplasmic and protection processes; of followed myelinated by (iii) neurons axonal [contact,1]. which leads to myelin wrapping— As OPCsensheathment differentiate of targeted into neuronal mature axons OLs with they ensuing undergo generation an of extensiveextremely electron development dense and of active compact myelin with an enduring (iv) long-term trophic and metabolic support system for cytoplasmicmaintenance reorganization and protection of cytoskeleton of myelinated neurons proteins [1]. and endoplasmic reticulum, which increases their intermediateAs OPCs cytoplasmic differentiate electroninto mature density OLs they and undergo helps an to extensive identify development them when of active studying with transmissioncytoplasmic electron reorganization microscopy of (TEM) cytoskeleton (Figure protei1). Identifyingns and endoplasmic characteristics reticulum, havewhich beenincreases presented in Part I Tabletheir 1 [5intermediate] as follows: cytoplasmic Oligodendrocytes electron density are an intermediated helps to identify in size them and when their studying thinned with cytoplasm transmission electron microscopy (TEM) (Figure 1). Identifying characteristics have been presented also have anin Part intermediate I Table 1 [5] as electron follows: Oligodendrocytes density that is helpfulare intermediate when in comparing size and their to thinned astrocytes cytoplasm and microglia. They alsoalso may have occur an inintermediate groups or electron nests anddensity are that more is helpful often foundwhen comparing in the white to astrocytes matter regionsand of the brain. In additionmicroglia. They to their also smallmay occur cytoplasmic in groups or volume, nests and theyare more have often multiple found in protoplasmic the white matter extensions, regions of the brain. In addition to their small cytoplasmic volume, they have multiple protoplasmic which allow OLs to concurrently myelinate multiple axons [1–4]. extensions, which allow OLs to concurrently myelinate multiple axons [1–4]. Figure 1. Comparison of astrocyte, ramified microglial cell, and oligodendrocyte to illustrate Figure 1. intermediateComparison electron of dens astrocyte,e and thin ramified cytoplasm. microglial(A) Depicts an cell, astrocyte and (AC) oligodendrocyte with electron lucent to illustrate intermediatecytoplasm electron and densea ramified and microglial thin cytoplasm. cell (rMGC) (withA) Depictsits electron an dense astrocyte cytoplasm. (AC) (B) with Illustrates electron a lucent cytoplasmthinned and a intermediate ramified microglial electron dense cell cytoplasm (rMGC) withof the its oligodendrocyte electron dense (OL) cytoplasm. obtained from (B )the Illustrates a thinned intermediatetransition zone electron in subcortical dense white cytoplasm matter (TZ of SCWM the oligodendrocyte) just deep to layer (OL)VI as compared obtained to from ACs and the transition microglia cells. Note that the OL is in the process of enwrapping at least 5 axons (1–5) with myelin in zone in subcortical(B) and its pseudo-colored white matter image, (TZSCWM) far right. Between just deep (A,B to) the layer cytoplasm VI as comparedhas been cut from to ACs each and cell microglia cells. Noteto that further the demonstrate OL is in the the processintermediate ofenwrapping electron (e) density at least of the 5 OL axons cytoplasm. (1–5) Also with note myelin the small in (B) and its pseudo-coloredamount image,of cytoplasm far right. as compared Between to nucleus (A,B) volume the cytoplasm as well as hasthe incorporation been cut from of myelin each at cell its to further demonstrateouter the margins intermediate of the cytoplasm electron plasmalemma. (e) density A ofpseudo-colorized the OL cytoplasm. image is Also inserted note far theright small to aid amount of in identifying OL nucleus (purple); cytoplasm (C green); fibrous astrocyte (fib AC blue); axons cytoplasm as compared to nucleus volume as well as the incorporation of myelin at its outer margins (yellow). Magnification ×3000; scale bar = 1 µm in A and 0.5 µm in (B). C: cytoplasm; MGC: microglial of the cytoplasmcell; M: myelin; plasmalemma. CKC: age-matched A pseudo-colorized non-diabetic wild image type control is inserted C57BL/KsJ. far right to aid in identifying OL nucleus (purple); cytoplasm (C green); fibrous astrocyte (fib AC blue); axons (yellow). Magnification ×3000; scaleThe bar small = 1cytoplasmicµm in A and volume 0.5 µ ofm oligodendrocyte in (B). C: cytoplasm; may be MGC: related microglial to its function cell; of M: constantly myelin; CKC: supplying its plasma membrane (up to three-times its volume of plasma membranes) in order to age-matched non-diabetic wild type control C57BL/KsJ. create the multiple myelin lamellar sheaths. These myelin lamella that enwrap multiple unmyelinated axons increase the speed of neuronal transmission of their action potentials via The smallmembrane cytoplasmic depolarization volume by high-density of oligodendrocyte voltage-gated sodium may be channels related that to creates its function the saltatory of constantly supplying(jumping) its plasma conduction membrane of their (up action to three-times potentials and its signaling volume at of the plasma nodes membranes)of Ranvier (Figure in order 1B). to create Importantly, this saltatory conduction allows electrical nerve signals to be propagated long distances the multipleat high myelin rates lamellarwithout any sheaths. degradation These of the myelin action lamellapotential thatsignaling enwrap [1–4]. multiple unmyelinated axons increase the speedMyelin of also neuronal serves as transmissiona protective sheath of theirof myelinated action potentialsneurons in order via membraneto provide for depolarizationlong- by high-densityterm axonal voltage-gated integrity and sodiummaintenance channels survival. thatMyelinated creates axons the are saltatory present in (jumping)
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