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The type IV Oligodendrocyte: experimental studies on chicken white matter
Linköping University, Department of Biomedicine and Surgery, Cell biology. Linköping University, Faculty of Health Sciences.
2002 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

In mammals, islet amyloid polypeptide (IAPP) is co-produced with insulin in pancreatic ß-cells. In the chicken, the expression of IAPP in the brain is more than 10-fold higher than in the pancreas. We made the fortuitous finding that a polyclonal rabbit antiserum raised against chicken IAPP did not recognise the immunogen, but labelled a subpopulation of oligodendroglia! cells in chicken white matter. The hitherto unknown antigen was called T4-O (Type 4 Oligodendrocyte) since it was localised to the Schwann cell-like Type IV oligodendrocyte of Del Rio-Hortega (1928). This formed a starting point for the present thesis, which is centred on the Type IV oligodendrocyte in chicken white matter.

Biochemical analysis of chicken spinal cord showed that the T4-O molecule is a protein with a molecular weight of approximately 100 kDa and an isoelectric point of about 4. Further characterisation has not yet been possible.

Immunohistochemical studies on frozen sections revealed that the white matter oligodendrocytes exhibit subpopulations expressing T4-O immunoreactivity strongly, weakly or not at all. Strongly T4-O immunoreactive (IR) oligodendrocytes are co-localised with thick myelinated fibres in the ventral (VF) and lateral funiculi of the spinal cord. A corresponding T4-O immunoreactivity is not found in the fish, the frog, the turtle, the rat and the rabbit.

To find out when the T4-0 antigen first appears during development we examined sections from embryonic and post-hatching chicken spinal cords by immunohistochemistry. This showed that the T4-O molecule is first expressed in the VF at embryonic day (E)15, after which the number of IR cells increases with age. Oligodendrocytes cultivated in vitro without or with neurons do not develop a T4-O IR phenotype.

These findings called for a closer analysis of the structural development of chicken VF white matter. Electron microscopic (EM) examination revealed a developmental sequence of events principally similar to the development of mammalian white matter, but with a more rapid time course. As seen in the electron microscope the first compact myelin has appeared by E12, when most oligodendrocytes are multipolar. By E15 it seems that these cells have developed a Type IV phenotype, possibly by eliminating some sheaths.

Histochemical analysis of Vibratome sections showed that Marchi-positive myelinoid bodies are enriched in white matter areas containing many T4-O IR oligodendrocytes and many large myelinated axons.

Examination of the three-dimensional (3D) anatomy of early VF oligodendrocytes in Vibratome slices after 04 labelling or after intracellular injection of a fluorescent dye revealed that these units indeed are Schwann cell-like, with a start length of around 50 µm. We also found that these sheaths expand very rapidly, reaching lengths exceeding 200 µm in three days (E12- E15). The 3D data conformed to our EM evidence that the early oligodendrocytes develop a unipolar Schwann cell-like Type IV anatomy through elimination of some sheaths.

To my knowledge the present observations represent the first evidence for an oligodendroglia! heterogeneity in the chicken spinal cord. Differences among oligodendrocytes might, conceivably, explain why inherited disorders of myelin metabolism such as Krabbe's disease, affect some CNS areas more than others.

Place, publisher, year, edition, pages
Linköping: Linköpings universitet , 2002. , 96 p.
Series
Linköping University Medical Dissertations, ISSN 0345-0082 ; 720
National Category
Medical and Health Sciences
Identifiers
URN: urn:nbn:se:liu:diva-25545Local ID: 9992ISBN: 91-7373-162-5 (print)OAI: oai:DiVA.org:liu-25545DiVA: diva2:245875
Public defence
2002-03-08, Berzeliussalen, Universitetssjukhuset, Linköping, 13:00 (Swedish)
Opponent
Available from: 2009-10-07 Created: 2009-10-07 Last updated: 2012-12-04Bibliographically approved
List of papers
1. Molecular heterogeneity of oligodendrocytes in chicken white matter
Open this publication in new window or tab >>Molecular heterogeneity of oligodendrocytes in chicken white matter
1999 (English)In: Glia, ISSN 0894-1491, E-ISSN 1098-1136, Vol. 27, no 1, 15-21 p.Article in journal (Refereed) Published
Abstract [en]

The classical studies by Del Rio Hortega (Mem. Real. Soc. Espan. Hist. Nat. 14:40–122, 1928) suggest that the oligodendrocyte population includes four morphological subtypes. Recent data from the cat and the rat show that the anatomy of oligodendrocytes related to early myelinating prospective large fibers differs from that of oligodendrocytes related to late myelinating prospective small fibers. After application of a polyclonal antiserum to cryostat sections from the chicken CNS, we noted that glial cells in the spinal cord white matter had become labeled. Analysis of the occurrence and cellular localization of this immunoreactivity—the T4-O immunoreactivity—in the CNS of the adult chicken showed that T4-O immunoreactive cells are enriched in the ventral funiculus and superficially in the lateral funiculus of the spinal cord, where they are co-localized with large fibers. Double staining with T4-O antiserum and anti-GFAP or the lectin BSI-B4 revealed that T4-O immunoreactive cells are not astrocytes or microglia. Staining with anti-HSP108, a general marker for avian oligodendrocytes, showed that T4-O immunoreactivity defines an oligodendroglial subpopulation. A search for T4-O immunoreactivity in spinal cord white matter of some other vertebrates revealed that T4-O immunoreactive cells are not present in sections from fish, frog, turtle, rat, and rabbit spinal cord white matter. These results suggest the presence of a fiber size-related molecular heterogeneity among chicken white matter oligodendrocytes.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-24854 (URN)10.1002/(SICI)1098-1136(199907)27:1<15::AID-GLIA2>3.0.CO;2-I (DOI)9254 (Local ID)9254 (Archive number)9254 (OAI)
Available from: 2009-10-07 Created: 2009-10-07 Last updated: 2017-12-13Bibliographically approved
2. Developing chicken oligodendrocytes express the type IV oligodendrocyte marker T4-O in situ, but not in vitro
Open this publication in new window or tab >>Developing chicken oligodendrocytes express the type IV oligodendrocyte marker T4-O in situ, but not in vitro
Show others...
2000 (English)In: Neuroscience Letters, ISSN 0304-3940, E-ISSN 1872-7972, Vol. 284, no 1-2, 21-24 p.Article in journal (Refereed) Published
Abstract [en]

Accumulating data suggest that the oligodendrocyte population includes morphological and biochemical subtypes. We recently reported that a polyclonal antiserum against an unknown antigen, the T4-O molecule, labels a subpopulation of chicken oligodendrocytes, obviously representing the type IV variety of Del Rio Hortega. The present study examines the developmental expression of the T4-O molecule in situ and in vitro. The results show that T4-O immunoreactive cells first appear at E15 in the ventral funiculus. But, oligodendrocytes cultured in vitro with or without neurones do not develop a T4-O immunoreactivity. We conclude that oligodendrocytes in the spinal cord of chicken embryos first express the T4-O molecule some time after onset of myelination, and that the T4-O immunoreactive phenotype does not develop in vitro.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-24853 (URN)10.1016/S0304-3940(00)00989-7 (DOI)9253 (Local ID)9253 (Archive number)9253 (OAI)
Available from: 2009-10-07 Created: 2009-10-07 Last updated: 2017-12-13Bibliographically approved
3. Myelination of prospective large fibres in chicken ventral funiculus
Open this publication in new window or tab >>Myelination of prospective large fibres in chicken ventral funiculus
2000 (English)In: Journal of Neurocytology, ISSN 0300-4864, E-ISSN 1573-7381, Vol. 29, no 10, 755-764 p.Article in journal (Refereed) Published
Abstract [en]

In mammals, the oligodendrocyte population includes morphological and molecular varieties. We reported previously that an antiserum against the T4-O molecule labels a subgroup of oligodendrocytes related to large myelinated axons in adult chicken white matter. We also reported that T4-O immunoreactive cells first appear in the developing ventral funiculus (VF) at embryonic day (E)15, subsequently increasing rapidly in number. Relevant fine structural data for comparison are not available in the literature. This prompted the present morphological analysis of developing and mature VF white matter in the chicken. The first axon-oligodendrocyte connections were seen at E10 and formation of compact myelin had started at E12. Between E12 and E15 the first myelinating oligodendrocytes attained a Schwann cell-like morphology. At hatching (E21) 60% of all VF axons were myelinated and in the adult this proportion had increased to 85%. The semilunar or polygonal oligodendrocytes associated with adult myelinated axons contained many organelles indicating a vivid metabolic activity. Domeshaped outbulgings with gap junction-like connections to astrocytic profiles were frequent. Oligodendrocytes surrounded by large myelinated axons and those surrounded by small myelinated axons were cytologically similar. But, thick and thin myelin sheaths had dissimilar periodicities and Marchi-positive myelinoid bodies occurred preferentially in relation to large myelinated axons. We conclude that early oligodendrocytes contact axons and form myelin well before the first expression of T4-O and that emergence of a T4-O immunoreactivity coincides in time with development of a Type IV phenotype. Our data also show that oligodendrocytes associated with thick axons are cytologically similar to cells related to thin axons. In addition, the development of chicken VF white matter was found to be similar to the development of mammalian white matter, except for the rapid time course.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-49235 (URN)10.1023/A:1010994505741 (DOI)
Available from: 2009-10-11 Created: 2009-10-11 Last updated: 2017-12-12Bibliographically approved
4. Morphology of early developing oligodendrocytes in the ventrolateral chicken spinal cord
Open this publication in new window or tab >>Morphology of early developing oligodendrocytes in the ventrolateral chicken spinal cord
(English)Manuscript (preprint) (Other academic)
Abstract [en]

As observed by Del Rio-Hortega (1928), the oligodendroglial population includes Type I and 11 cells related to several thin axons, Type III cells with a few processes in relation to relatively thick axons and Type IV cells related to a single thick axon. This structural diversity of oligodendrocytes is accompanied by a molecular heterogeneity. In the chicken spinal cord oligodendrocytes have begun to contact axons at embryonic day (E)10 and compact sheaths have appeared by E12. AI the latter stage, most sheath-forming oligodendrocytes contact more than one axon. At E15, however, each sheath-forming cell seems to have developed a Schwann cell-like anatomy, being related to a single axon. Against this background, the present study examines the 3D anatomy of early developing oligodendrocytes in the chicken spinal cord. Examination of slices immunostained with antibodies against the oligodendroglial marker 04 showed that a few positive cells are at hand at E6, after which the occurrence increases with age. At E12 most immunostained cells have two or more processes. At E15 however, dye-injected oligodendrocytes have developed a Type IV structure. Between E12 and E15, mean sheath length increases some 4x, from 50 µm to over 200 flm, while the length of the spinal cord increases 36% only. Hence, early oligodendrocytes in chicken white matter develop a Type IV anatomy between E12 and E15 through an elimination of sheaths.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-81479 (URN)
Available from: 2012-09-17 Created: 2012-09-17 Last updated: 2012-09-17Bibliographically approved

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