Diversity amongst the microglia in growing and regenerating fish CNS: Immunohistochemical characterization using FL. 1, an anti‐macrophage monoclonal antibody

We have immunohistochemically characterized the forms and distribution of microglia—the macrophages of the CNS—in fish, using a new monoclonal antibody (mAb), FL.1. This mAb specifically reacts with resident macrophages throughout the body in Oreochromine fish, including Kupffer cells, gut‐associated myeloid cells, and peritoneal macrophages, as well as with microglia, but circulating monocytes are not labelled with FL.1. The FL.1‐epitope, which is lost following treatment with reducing agents, has an extracellular location and is associated with three integral membrane glycoprotein variants.

[1]  V. Perry,et al.  Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers , 1983, The Journal of cell biology.

[2]  J. Scholes Nerve fibre topography in the retinal projection to the tectum , 1979, Nature.

[3]  J. Scholes,et al.  Glial domains and nerve fiber patterns in the fish retinotectal pathway , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Michael L. Dustin,et al.  T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1 , 1989, Nature.

[5]  J. Cronly-Dillon,et al.  Glial fibrillary acidic protein (GFAP) from goldfish: Its localisation in visual pathway , 1989, Glia.

[6]  R. Skoff The fine structure of pulse labeled (3H‐thymidine cells) in degenerating rat optic nerve , 1975, The Journal of comparative neurology.

[7]  A. Peters,et al.  A third neuroglial cell types. An electron microscopic study , 1968, The Journal of comparative neurology.

[8]  T. Springer,et al.  Cloning of the β subunit of the leukocyte adhesion proteins: Homology to an extracellular matrix receptor defines a novel supergene family , 1987, Cell.

[9]  P. Bartlett Pluripotential hemopoietic stem cells in adult mouse brain. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[10]  V. Perry,et al.  Plasma membrane receptors of the mononuclear phagocyte system , 1988, Journal of Cell Science.

[11]  F. Sánchez‐Madrid,et al.  A human leukocyte differentiation antigen family with distinct alpha- subunits and a common beta-subunit: the lymphocyte function-associated antigen (LFA-1), the C3bi complement receptor (OKM1/Mac-1), and the p150,95 molecule , 1983, The Journal of experimental medicine.

[12]  A. Willis,et al.  The primary structure of the beta‐subunit of the cell surface adhesion glycoproteins LFA‐1, CR3 and p150,95 and its relationship to the fibronectin receptor. , 1987, The EMBO journal.

[13]  J. Schnitzer Enzyme‐histochemical demonstration of microglial cells in the adult and postnatal rabbit retina , 1989, The Journal of comparative neurology.

[14]  R. Hynes,et al.  Antibodies to the conserved cytoplasmic domain of the integrin beta 1 subunit react with proteins in vertebrates, invertebrates, and fungi , 1988, The Journal of cell biology.

[15]  H. Wiśniewski,et al.  The role of oligodendroglia and astroglia in Wallerian degeneration of the optic nerve. , 1973, Brain research.

[16]  C. P. Leblond,et al.  Radioautographic investigation of gliogenesis in the corpus callosum of young rats II. Origin of microglial cells , 1978, The Journal of comparative neurology.

[17]  D. Giulian,et al.  Interleukin-1 is an astroglial growth factor in the developing brain , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  M. Graeber,et al.  The microglial cytoskeleton: vimentin is localized within activated cellsin situ , 1988, Journal of neurocytology.

[19]  W. Hickey,et al.  Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. , 1988, Science.

[20]  T. Springer,et al.  Leukocyte adhesion deficiency: an inherited defect in the Mac-1, LFA-1, and p150,95 glycoproteins. , 1987, Annual review of medicine.

[21]  P. Dawson,et al.  Induction of rat E and chicken A-I apolipoproteins and mRNAs during optic nerve degeneration. , 1986, The Journal of biological chemistry.

[22]  K. Hancock,et al.  India ink staining of proteins on nitrocellulose paper. , 1983, Analytical biochemistry.

[23]  R. Geha,et al.  Phosphorylation of T cell membrane proteins by activators of protein kinase C. , 1988, Journal of immunology.

[24]  E. Egberts,et al.  Separation of lymphocyte subpopulations in carp Cyprinus carpio L. by monoclonal antibodies: immunohistochemical studies. , 1983, Immunology.

[25]  E. Glasgow,et al.  A type II keratin is expressed in glial cells of the goldfish visual pathway , 1989, Neuron.

[26]  M. Graeber,et al.  Functional plasticity of microglia: A review , 1988, Glia.

[27]  N. Baumann,et al.  Distribution of radioactivity in myelin lipids following subcutaneous injection of [14C]stearate. , 1978, Biochimica et biophysica acta.

[28]  Blakemore Wf The ultrastructure of the subependymal plate in the rat. , 1969 .

[29]  M. Graeber,et al.  Microglial cells but not astrocytes undergo mitosis following rat facial nerve axotomy , 1988, Neuroscience Letters.

[30]  M. Edidin,et al.  Hydrophobic adsorption chromatography to reduce nonspecific staining by rhodamine-labeled antibodies. , 1986, Analytical biochemistry.

[31]  A. Springer,et al.  Light microscopic study of degenerating cobalt‐filled optic axons in goldfish: Role of microglia and radial glia in debris removal , 1989, The Journal of comparative neurology.

[32]  L. Lachman,et al.  Interleukin-1 stimulation of astroglial proliferation after brain injury. , 1985, Science.

[33]  C. Katagiri,et al.  Ontogeny and tissue distribution of leukocyte-common antigen bearing cells during early development of Xenopus laevis. , 1989, Development.

[34]  P. Lazarow,et al.  Immunoblotting of hydrophobic integral membrane proteins. , 1988, Analytical biochemistry.

[35]  J. Markl,et al.  Localization of cytokeratins in tissues of the rainbow trout: fundamental differences in expression pattern between fish and higher vertebrates. , 1988, Differentiation; research in biological diversity.

[36]  M. Graeber,et al.  Identity of ED2‐positive perivascular cells in rat brain , 1989, Journal of neuroscience research.

[37]  D. Young,et al.  Brain peptides and glial growth. II. Identification of cells that secrete glia-promoting factors , 1986, The Journal of cell biology.

[38]  D. Giulian,et al.  Colony-stimulating factors as promoters of ameboid microglia , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  Takurou Kobayashi,et al.  Donor-derived cells in the central nervous system of twitcher mice after bone marrow transplantation. , 1988, Science.

[40]  G. Innocenti,et al.  Transitory macrophages in the white matter of the developing visual cortex. I. Light and electron microscopic characteristics and distribution. , 1983, Brain research.

[41]  M. Schwartz,et al.  Regenerating fish optic nerves and a regeneration-like response in injured optic nerves of adult rabbits. , 1985, Science.

[42]  V. Perry,et al.  Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain , 1985, Neuroscience.

[43]  R. Mahley,et al.  Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins. , 1987, Biochimica et biophysica acta.

[44]  D. De Rijk,et al.  Involvement of LFA-1 in lymphoma invasion and metastasis demonstrated with LFA-1-deficient mutants , 1989, The Journal of cell biology.

[45]  R. Hynes,et al.  Xenopus laevis integrins. Structural conservation and evolutionary divergence of integrin beta subunits. , 1988, The Journal of biological chemistry.

[46]  J. Scholes,et al.  Reticular astrocytes in the fish optic nerve: macroglia with epithelial characteristics form an axially repeated lacework pattern, to which nodes of Ranvier are apposed , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  M. Murray Regeneration of retinal axons into the goldfish optic tectum , 1976, The Journal of comparative neurology.

[48]  D. Giulian Peptides from the regenerating central nervous system of goldfish stimulate glia. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[49]  J. Taylor,et al.  Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. , 1985, The Journal of clinical investigation.

[50]  M. Murray,et al.  Transport of protein in goldfish optic nerve during regeneration. , 1969, Experimental neurology.

[51]  J. Harris,et al.  The ontogeny of gut‐associated lymphoid tissue in Oreochromis‐mossambicus , 1987 .

[52]  D. Mason,et al.  Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. , 1986, Immunology.

[53]  M. Schwartz,et al.  Optic Nerve Regeneration in Adult Fish and Apolipoprotein A‐I , 1989, Journal of neurochemistry.

[54]  R. Sperry,et al.  Preferential selection of central pathways by regenerating optic fibers. , 1963, Experimental neurology.

[55]  M. Graeber,et al.  Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells , 1988, Journal of neuroscience research.

[56]  J. August,et al.  The human lymphocyte function-associated (HLFA) antigen and a related macrophage differentiation antigen (HMac-1): functional effects of subunit-specific monoclonal antibodies. , 1985, Journal of immunology.

[57]  H. Towbin,et al.  Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[58]  J. Cammermeyer The life history of the microglial cell: a light microscopic study. , 1970, Neurosciences research.

[59]  T. Springer,et al.  Heterogeneous mutations in the β subunit common to the LFA-1, Mac-1, and p150,95 glycoproteins cause leukocyte adhesion deficiency , 1987, Cell.

[60]  P. Gebicke-haerter,et al.  Lipopolysaccharide-free conditions in primary astrocyte cultures allow growth and isolation of microglial cells , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.