Skip to main content
SpringerLink
Log in

Evolution of Neuroglia

  • Chapter
  • First Online:
Neuroglia in Neurodegenerative Diseases

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1175))

Abstract

As the nervous system evolved from the diffused to centralised form, the neurones were joined by the appearance of the supportive cells, the neuroglia. Arguably, these non-neuronal cells evolve into a more diversified cell family than the neurones are. The first ancestral neuroglia appeared in flatworms being mesenchymal in origin. In the nematode C. elegans proto-astrocytes/supportive glia of ectodermal origin emerged, albeit the ensheathment of axons by glial cells occurred later in prawns. The multilayered myelin occurred by convergent evolution of oligodendrocytes and Schwann cells in vertebrates above the jawless fishes. Nutritive partitioning of the brain from the rest of the body appeared in insects when the hemolymph-brain barrier, a predecessor of the blood-brain barrier was formed. The defensive cellular mechanism required specialisation of bona fide immune cells, microglia, a process that occurred in the nervous system of leeches, bivalves, snails, insects and above. In ascending phylogeny, new type of glial cells, such as scaffolding radial glia, appeared and as the bran sizes enlarged, the glia to neurone ratio increased. Humans possess some unique glial cells not seen in other animals.

Is evolution a theory, a system or a hypothesis? It is much more - it is a general postulate to which all theories, all hypotheses, all systems must henceforward bow and which they must satisfy in order to be thinkable and true. Evolution is a light which illuminates all facts, a trajectory which all lines of thought must follow-this is what evolution is.

Pierre Teilhard de Chardin.

quoted from Theodosius Dobzhansky, Nothing in Biology Makes Sense Except in the Light of Evolution, The American Biology Teacher, Vol. 35, No. 3 (Mar., 1973), pp. 125–129.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Altun ZF, Chen B, Wang ZW, Hall DH (2009) High resolution map of Caenorhabditis elegans gap junction proteins. Dev Dyn 238:1936–1950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Ari C, Kalman M (2008) Evolutionary changes of astroglia in Elasmobranchii comparing to amniotes: a study based on three immunohistochemical markers (GFAP, S-100, and glutamine synthetase). Brain Behav Evol 71:305–324

    Article  PubMed  Google Scholar 

  3. Awasaki T, Lai SL, Ito K, Lee T (2008) Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci 28:13742–13753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bacaj T, Tevlin M, Lu Y, Shaham S (2008) Glia are essential for sensory organ function in C. elegans. Science 322:744–747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bahney J, von Bartheld CS (2018) The cellular composition and glia-neuron ratio in the spinal cord of a human and a nonhuman primate: comparison with other species and brain regions. Anat Rec (Hoboken) 301:697–710

    Article  Google Scholar 

  6. Bainton RJ, Tsai LT, Schwabe T, DeSalvo M, Gaul U, Heberlein U (2005) Moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 123:145–156

    Article  CAS  PubMed  Google Scholar 

  7. Baumgart EV, Barbosa JS, Bally-Cuif L, Gotz M, Ninkovic J (2010) Stab wound injury of the zebrafish telencephalon: a model for comparative analysis of reactive gliosis. Glia 60:343–357

    Article  Google Scholar 

  8. Baumgartner S, Littleton JT, Broadie K, Bhat MA, Harbecke R, Lengyel JA, Chiquet-Ehrismann R, Prokop A, Bellen HJ (1996) A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87:1059–1068

    Article  CAS  PubMed  Google Scholar 

  9. Beckervordersandforth RM, Rickert C, Altenhein B, Technau GM (2008) Subtypes of glial cells in the Drosophila embryonic ventral nerve cord as related to lineage and gene expression. Mech Dev 125:542–557

    Article  CAS  PubMed  Google Scholar 

  10. Bedini C, Lanfranchi A (1991) The central and peripheral nervous system of Acoela (plathelminthes). An electron microscopical study. Acta Zoologica (Stockholm) 72:101–106

    Article  Google Scholar 

  11. Bery A, Cardona A, Martinez P, Hartenstein V (2010) Structure of the central nervous system of a juvenile acoel, Symsagittifera roscoffensis. Dev Genes Evol 220:61–76

    Article  PubMed  PubMed Central  Google Scholar 

  12. Booth GE, Kinrade EF, Hidalgo A (2000) Glia maintain follower neuron survival during Drosophila CNS development. Development 127:237–244

    CAS  PubMed  Google Scholar 

  13. Borycz J, Borycz JA, Loubani M, Meinertzhagen IA (2002) tan and ebony genes regulate a novel pathway for transmitter metabolism at fly photoreceptor terminals. J Neurosci 22:10549–10557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Buchanan RL, Benzer S (1993) Defective glia in the Drosophila brain degeneration mutant drop-dead. Neuron 10:839–850

    Article  CAS  PubMed  Google Scholar 

  15. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Butler AB, Hodos W (2005) Vertebrate neuroanatomy: evolution and adaptation, 2nd edn. Wiley, New York

    Book  Google Scholar 

  17. Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev Camb Philos Soc 73:203–266

    Article  CAS  PubMed  Google Scholar 

  18. Cavalier-Smith T (2009) Megaphylogeny, cell body plans, adaptive zones: causes and timing of eukaryote basal radiations. J Eukaryot Microbiol 56:26–33

    Article  PubMed  Google Scholar 

  19. Chaturvedi R, Reddig K, Li HS (2014) Long-distance mechanism of neurotransmitter recycling mediated by glial network facilitates visual function in Drosophila. Proc Natl Acad Sci USA 111:2812–2817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Chell JM, Brand AH (2010) Nutrition-responsive glia control exit of neural stem cells from quiescence. Cell 143:1161–1173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Christensen JR, Larsen KB, Lisanby SH, Scalia J, Arango V, Dwork AJ, Pakkenberg B (2007) Neocortical and hippocampal neuron and glial cell numbers in the rhesus monkey. Anat Rec (Hoboken) 290:330–340

    Article  Google Scholar 

  22. Coggeshall RE, Fawcett DW (1964) The fine structure of the central nervous system of the leech, Hirudo Medicinalis. J Neurophysiol 27:229–289

    Article  CAS  PubMed  Google Scholar 

  23. Colombo JA, Reisin HD (2004) Interlaminar astroglia of the cerebral cortex: a marker of the primate brain. Brain Res 1006:126–131

    Article  CAS  PubMed  Google Scholar 

  24. Colombo JA, Sherwood CC, Hof PR (2004) Interlaminar astroglial processes in the cerebral cortex of great apes. Anat Embryol (Berl) 208:215–218

    Article  Google Scholar 

  25. Colombo JA, Yanez A, Puissant V, Lipina S (1995) Long, interlaminar astroglial cell processes in the cortex of adult monkeys. J Neurosci Res 40:551–556

    Article  CAS  PubMed  Google Scholar 

  26. Csoknya M, Dénes V, Wilhelm M (2012) Glial cells in the central nervous system of earthworm, Eisenia fetida. Acta Biol Hung 63(Suppl. 1):114–128

    Article  PubMed  Google Scholar 

  27. De Pinto V, Caggese C, Prezioso G, Ritossa F (1987) Purification of the glutamine synthetase II isozyme of Drosophila melanogaster and structural and functional comparison of glutamine synthetases I and II. Biochem Genet 25:821–836

    Article  PubMed  Google Scholar 

  28. Deitmer JW (1991) Electrogenic sodium-dependent bicarbonate secretion by glial cells of the leech central nervous system. J Gen Physiol 98:637–655

    Article  CAS  PubMed  Google Scholar 

  29. Deitmer JW, Kristan WB Jr (1999) Glial responses during evoked behaviors in the leech. Glia 26:186–189

    Article  CAS  PubMed  Google Scholar 

  30. Deitmer JW, Rose CR, Munsch T, Schmidt J, Nett W, Schneider HP, Lohr C (1999) Leech giant glial cell: functional role in a simple nervous system. Glia 28:175–182

    Article  CAS  PubMed  Google Scholar 

  31. Deitmer JW, Schlue WR (1987) The regulation of intracellular pH by identified glial cells and neurones in the central nervous system of the leech. J Physiol 388:261–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Deitmer JW, Schlue WR (1989) An inwardly directed electrogenic sodium-bicarbonate co-transport in leech glial cells. J Physiol 411:179–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Deitmer JW, Schneider HP (1997) Intracellular acidification of the leech giant glial cell evoked by glutamate and aspartate. Glia 19:111–122

    Article  CAS  PubMed  Google Scholar 

  34. Deitmer JW, Verkhratsky AJ, Lohr C (1998) Calcium signalling in glial cells. Cell Calcium 24:405–416

    Article  CAS  PubMed  Google Scholar 

  35. DeSalvo MK, Mayer N, Mayer F, Bainton RJ (2011) Physiologic and anatomic characterization of the brain surface glia barrier of Drosophila. Glia 59:1322–1340

    Article  PubMed  PubMed Central  Google Scholar 

  36. Doherty J, Logan MA, Tasdemir OE, Freeman MR (2009) Ensheathing glia function as phagocytes in the adult Drosophila brain. J Neurosci 29:4768–4781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Dykes IM, Freeman FM, Bacon JP, Davies JA (2004) Molecular basis of gap junctional communication in the CNS of the leech Hirudo medicinalis. J Neurosci 24:886–894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ebens AJ, Garren H, Cheyette BN, Zipursky SL (1993) The Drosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74:15–27

    Article  CAS  PubMed  Google Scholar 

  39. Edwards TN, Meinertzhagen IA (2010) The functional organisation of glia in the adult brain of Drosophila and other insects. Prog Neurobiol 90:471–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Eriksen N, Pakkenberg B (2007) Total neocortical cell number in the mysticete brain. Anat Rec (Hoboken) 290:83–95

    Article  Google Scholar 

  41. Felton CM, Johnson CM (2011) Modulation of dopamine-dependent behaviors by the Caenorhabditis elegans Olig homolog HLH-17. J Neurosci Res 89:1627–1636

    Article  CAS  PubMed  Google Scholar 

  42. Fernandez I, Pardos F, Benito J, Roldan C (1996) Ultrastructural observations on the phoronid nervous system. J Morphol 230:265–281

    Article  PubMed  Google Scholar 

  43. Freeman MR, Doherty J (2006) Glial cell biology in Drosophila and vertebrates. Trends Neurosci 29:82–90

    Article  CAS  PubMed  Google Scholar 

  44. Genova JL, Fehon RG (2003) Neuroglian, Gliotactin, and the Na+/K+ATPase are essential for septate junction function in Drosophila. J Cell Biol 161:979–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ghysen A (2003) The origin and evolution of the nervous system. Int J Dev Biol 47:555–562

    PubMed  Google Scholar 

  46. Gobron S, Monnerie H, Meiniel R, Creveaux I, Lehmann W, Lamalle D, Dastugue B, Meiniel A (1996) SCO-spondin: a new member of the thrombospondin family secreted by the subcommissural organ is a candidate in the modulation of neuronal aggregation. J Cell Sci 109(Pt 5):1053–1061

    CAS  PubMed  Google Scholar 

  47. Grosjean Y, Grillet M, Augustin H, Ferveur JF, Featherstone DE (2008) A glial amino-acid transporter controls synapse strength and courtship in Drosophila. Nat Neurosci 11:54–61

    Article  CAS  PubMed  Google Scholar 

  48. Grupp L, Wolburg H, Mack AF (2010) Astroglial structures in the zebrafish brain. J Comp Neurol 518:4277–4287

    Article  CAS  PubMed  Google Scholar 

  49. Hartenstein V (2011) Morphological diversity and development of glia in Drosophila. Glia 59:1237–1252

    Article  PubMed  PubMed Central  Google Scholar 

  50. Hatan M, Shinder V, Israeli D, Schnorrer F, Volk T (2011) The Drosophila blood brain barrier is maintained by GPCR-dependent dynamic actin structures. J Cell Biol 192:307–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Hawkins A, Olszewski J (1957) Glia/nerve cell index for cortex of the whale. Science 126:76–77

    Article  CAS  PubMed  Google Scholar 

  52. Hedgecock EM, Culotti JG, Hall DH (1990) The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4:61–85

    Article  CAS  PubMed  Google Scholar 

  53. Heiman MG, Shaham S (2009) DEX-1 and DYF-7 establish sensory dendrite length by anchoring dendritic tips during cell migration. Cell 137:344–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Helm C, Karl A, Beckers P, Kaul-Strehlow S, Ulbricht E, Kourtesis I, Kuhrt H, Hausen H, Bartolomaeus T, Reichenbach A, Bleidorn C (2017) Early evolution of radial glial cells in Bilateria. Proc Biol Sci 284

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  55. Heuser JE, Doggenweiler CF (1966) The fine structural organization of nerve fibers, sheaths, and glial cells in the prawn, Palaemonetes vulgaris. J Cell Biol 30:381–403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hirth IC, Deitmer JW (2006) 5-Hydroxytryptamine-mediated increase in glutamate uptake by the leech giant glial cell. Glia 54:786–794

    Article  PubMed  Google Scholar 

  57. Hodgkin AL (1954) A note on conduction velocity. J Physiol 125:221–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Holland ND (2003) Early central nervous system evolution: an era of skin brains? Nat Rev Neurosci 4:617–627

    Article  CAS  PubMed  Google Scholar 

  59. Holmgren E (1901) Beiträge zur Morphologie der Zelle: I. Nervenzellen. Anat Hefte 18:267–326

    Article  Google Scholar 

  60. Hosoya T, Takizawa K, Nitta K, Hotta Y (1995) glial cells missing: a binary switch between neuronal and glial determination in Drosophila. Cell 82:1025–1036

    Article  CAS  PubMed  Google Scholar 

  61. Igaki T, Kanda H, Yamamoto-Goto Y, Kanuka H, Kuranaga E, Aigaki T, Miura M (2002) Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J 21:3009–3018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Jelsing J, Nielsen R, Olsen AK, Grand N, Hemmingsen R, Pakkenberg B (2006) The postnatal development of neocortical neurons and glial cells in the Gottingen minipig and the domestic pig brain. J Exp Biol 209:1454–1462

    Article  PubMed  Google Scholar 

  63. Jones BW, Fetter RD, Tear G, Goodman CS (1995) glial cells missing: a genetic switch that controls glial versus neuronal fate. Cell 82:1013–1023

    Article  CAS  PubMed  Google Scholar 

  64. Kanda H, Igaki T, Kanuka H, Yagi T, Miura M (2002) Wengen, a member of the Drosophila tumor necrosis factor receptor superfamily, is required for Eiger signaling. J Biol Chem 277:28372–28375

    Article  CAS  PubMed  Google Scholar 

  65. Kandarian B, Sethi J, Wu A, Baker M, Yazdani N, Kym E, Sanchez A, Edsall L, Gaasterland T, Macagno E (2012) The medicinal leech genome encodes 21 innexin genes: different combinations are expressed by identified central neurons. Dev Genes Evol 222:29–44

    Article  CAS  PubMed  Google Scholar 

  66. Kawano T, Takuwa K, Kuniyoshi H, Juni N, Nakajima T, Yamamoto D, Kimura Y (1999) Cloning and characterization of a Drosophila melanogaster cDNA encoding a glutamate transporter. Biosci Biotechnol Biochem 63:2042–2044

    Article  CAS  PubMed  Google Scholar 

  67. Keller LC, Cheng L, Locke CJ, Muller M, Fetter RD, Davis GW (2011) Glial-derived prodegenerative signaling in the Drosophila neuromuscular system. Neuron 72:760–775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91:461–553

    Article  CAS  PubMed  Google Scholar 

  69. Kim J, Jones BW, Zock C, Chen Z, Wang H, Goodman CS, Anderson DJ (1998) Isolation and characterization of mammalian homologs of the Drosophila gene glial cells missing. Proc Natl Acad Sci USA 95:12364–12369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kremer MC, Jung C, Batelli S, Rubin GM, Gaul U (2017) The glia of the adult Drosophila nervous system. Glia 65:606–638

    Article  PubMed  PubMed Central  Google Scholar 

  71. Kretzschmar D, Hasan G, Sharma S, Heisenberg M, Benzer S (1997) The swiss cheese mutant causes glial hyperwrapping and brain degeneration in Drosophila. J Neurosci 17:7425–7432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Kurant E (2011) Keeping the CNS clear: glial phagocytic functions in Drosophila. Glia 59:1304–1311

    Article  PubMed  Google Scholar 

  73. Kurshan PT, Oztan A, Schwarz TL (2009) Presynaptic alpha2delta-3 is required for synaptic morphogenesis independent of its Ca2+-channel functions. Nat Neurosci 12:1415–1423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Kusano K (1966) Electrical activity and structural correlates of giant nerve fibers in Kuruma shrimp (Penaeus japonicus). J Cell Physiol 68:361–383

    Article  Google Scholar 

  75. Labouesse M, Sookhareea S, Horvitz HR (1994) The Caenorhabditis elegans gene lin-26 is required to specify the fates of hypodermal cells and encodes a presumptive zinc-finger transcription factor. Development 120:2359–2368

    CAS  PubMed  Google Scholar 

  76. Le Marrec-Croq F, Drago F, Vizioli J, Sautiere PE, Lefebvre C (2013) The leech nervous system: a valuable model to study the microglia involvement in regenerative processes. Clin Dev Immunol 2013:274019

    PubMed  PubMed Central  Google Scholar 

  77. Lidow MS, Song ZM (2001) Primates exposed to cocaine in utero display reduced density and number of cerebral cortical neurons. J Comp Neurol 435:263–275

    Article  CAS  PubMed  Google Scholar 

  78. Lievens JC, Rival T, Iche M, Chneiweiss H, Birman S (2005) Expanded polyglutamine peptides disrupt EGF receptor signaling and glutamate transporter expression in Drosophila. Hum Mol Genet 14:713–724

    Article  CAS  PubMed  Google Scholar 

  79. Lohr C, Deitmer JW (1997) Structural and physiological properties of leech giant glial cells as studied by confocal microscopy. Exp Biol Online 2:8

    Article  Google Scholar 

  80. Lohr C, Deitmer JW (2006) Calcium signaling in invertebrate glial cells. Glia 54:642–649

    Article  PubMed  Google Scholar 

  81. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR (2006) The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50:869–881

    Article  CAS  PubMed  Google Scholar 

  82. Magistretti PJ (2009) Neuroscience. Low-cost travel in neurons. Science 325:1349–1351

    Article  CAS  PubMed  Google Scholar 

  83. Mashanov VS, Zueva OR, Garcia-Arraras JE (2010) Organization of glial cells in the adult sea cucumber central nervous system. Glia 58:1581–1593

    Article  PubMed  Google Scholar 

  84. Mashanov VS, Zueva OR, Heinzeller T, Aschauer B, Naumann WW, Grondona JM, Cifuentes M, Garcia-Arraras JE (2009) The central nervous system of sea cucumbers (Echinodermata: Holothuroidea) shows positive immunostaining for a chordate glial secretion. Front Zool 6:11

    Article  PubMed  PubMed Central  Google Scholar 

  85. Mayer F, Mayer N, Chinn L, Pinsonneault RL, Kroetz D, Bainton RJ (2009) Evolutionary conservation of vertebrate blood-brain barrier chemoprotective mechanisms in Drosophila. J Neurosci 29:3538–3550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. McMiller TL, Johnson CM (2005) Molecular characterization of HLH-17, a C. elegans bHLH protein required for normal larval development. Gene 356:1–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Meinertzhagen IA, O’Neil SD (1991) Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J Comp Neurol 305:232–263

    Article  CAS  PubMed  Google Scholar 

  88. Melom JE, Littleton JT (2013) Mutation of a NCKX eliminates glial microdomain calcium oscillations and enhances seizure susceptibility. J Neurosci 33:1169–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Morante J, Vallejo DM, Desplan C, Dominguez M (2013) Conserved miR-8/miR-200 defines a glial niche that controls neuroepithelial expansion and neuroblast transition. Dev Cell 27:174–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Morrison SJ, Spradling AC (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132:598–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Mortensen HS, Pakkenberg B, Dam M, Dietz R, Sonne C, Mikkelsen B, Eriksen N (2014) Quantitative relationships in delphinid neocortex. Front Neuroanat 8:132

    Article  PubMed  PubMed Central  Google Scholar 

  92. Muller M, Henrich A, Klockenhoff J, Dierkes PW, Schlue WR (2000) Effects of ATP and derivatives on neuropile glial cells of the leech central nervous system. Glia 29:191–201

    Article  CAS  PubMed  Google Scholar 

  93. Munsch T, Deitmer JW (1992) Calcium transients in identified leech glial cells in situ evoked by high potassium concentrations and 5-hydroxytryptamine. J Exp Biol 167:251–265

    CAS  PubMed  Google Scholar 

  94. Nave KA, Werner HB (2014) Myelination of the nervous system: mechanisms and functions. Annu Rev Cell Dev Biol 30:503–533

    Article  CAS  PubMed  Google Scholar 

  95. Nedergaard M (1994) Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263:1768–1771

    Article  CAS  PubMed  Google Scholar 

  96. Ng FS, Tangredi MM, Jackson FR (2011) Glial cells physiologically modulate clock neurons and circadian behavior in a calcium-dependent manner. Curr Biol 21:625–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Nicholls JG, Kuffler SW (1964) Extracellular space as a pathway for exchange between blood and neurons in the central nervous system of the leech: ionic composition of glial cells and neurons. J Neurophysiol 27:645–671

    Article  CAS  PubMed  Google Scholar 

  98. Oberheim NA, Goldman SA, Nedergaard M (2012) Heterogeneity of astrocytic form and function. Methods Mol Biol 814:23–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, Ransom BR, Goldman SA, Nedergaard M (2009) Uniquely hominid features of adult human astrocytes. J Neurosci 29:3276–3287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Oberheim NA, Wang X, Goldman S, Nedergaard M (2006) Astrocytic complexity distinguishes the human brain. Trends Neurosci 29:547–553

    Article  CAS  PubMed  Google Scholar 

  101. Oikonomou G, Shaham S (2011) The glia of Caenorhabditis elegans. Glia 59:1253–1263

    Article  PubMed  Google Scholar 

  102. Oikonomou G, Shaham S (2012) On the morphogenesis of glial compartments in the sensory organs of Caenorhabditis elegans. Worm 1:51–55

    Article  PubMed  PubMed Central  Google Scholar 

  103. Oland LA, Gibson NJ, Tolbert LP (2010) Localization of a GABA transporter to glial cells in the developing and adult olfactory pathway of the moth Manduca sexta. J Comp Neurol 518:815–838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Omoto JJ, Lovick JK, Hartenstein V (2016) Origins of glial cell populations in the insect nervous system. Curr Opin Insect Sci 18:96–104

    Article  PubMed  PubMed Central  Google Scholar 

  105. Pakhotin P, Verkhratsky A (2005) Electrical synapses between Bergmann glial cells and Purkinje neurones in rat cerebellar slices. Mol Cell Neurosci 28:79–84

    Article  PubMed  Google Scholar 

  106. Pakkenberg B, Gundersen HJ (1988) Total number of neurons and glial cells in human brain nuclei estimated by the disector and the fractionator. J Microsc 150:1–20

    Article  CAS  PubMed  Google Scholar 

  107. Pakkenberg B, Gundersen HJ (1997) Neocortical neuron number in humans: effect of sex and age. J Comp Neurol 384:312–320

    Article  CAS  PubMed  Google Scholar 

  108. Parker RJ, Auld VJ (2006) Roles of glia in the Drosophila nervous system. Semin Cell Dev Biol 17:66–77

    Article  CAS  PubMed  Google Scholar 

  109. Paterson JR, Garcia-Bellido DC, Lee MS, Brock GA, Jago JB, Edgecombe GD (2011) Acute vision in the giant Cambrian predator Anomalocaris and the origin of compound eyes. Nature 480:237–240

    Article  CAS  PubMed  Google Scholar 

  110. Pentreath VW, Radojcic T, Seal LH, Winstanley EK (1985) The glial cells and glia-neuron relations in the buccal ganglia of Planorbis corneus (L.): cytological, qualitative and quantitative changes during growth and ageing. Philos Trans R Soc Lond B Biol Sci 307:399–455

    Article  CAS  PubMed  Google Scholar 

  111. Pereanu W, Spindler S, Cruz L, Hartenstein V (2007) Tracheal development in the Drosophila brain is constrained by glial cells. Dev Biol 302:169–180

    Article  CAS  PubMed  Google Scholar 

  112. Perens EA, Shaham S (2005) C. elegans daf-6 encodes a patched-related protein required for lumen formation. Dev Cell 8:893–906

    Article  CAS  PubMed  Google Scholar 

  113. Popescu LM, Faussone-Pellegrini MS (2010) TELOCYTES—a case of serendipity: the winding way from Interstitial Cells of Cajal (ICC), via Interstitial Cajal-Like Cells (ICLC) to TELOCYTES. J Cell Mol Med 14:729–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Procko C, Shaham S (2010) Assisted morphogenesis: glial control of dendrite shapes. Curr Opin Cell Biol 22:560–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Rabinowitch I, Chatzigeorgiou M, Schafer WR (2013) A gap junction circuit enhances processing of coincident mechanosensory inputs. Curr Biol 23:963–967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Rakic P (2003) Elusive radial glial cells: historical and evolutionary perspective. Glia 43:19–32

    Article  PubMed  Google Scholar 

  117. Reichenbach A (1989) Glia:neuron index: review and hypothesis to account for different values in various mammals. Glia 2:71–77

    Article  CAS  PubMed  Google Scholar 

  118. Reichenbach A, Neumann M, Bruckner G (1987) Cell length to diameter relation of rat fetal radial glia–does impaired K+ transport capacity of long thin cells cause their perinatal transformation into multipolar astrocytes? Neurosci Lett 73:95–100

    Article  CAS  PubMed  Google Scholar 

  119. Reichenbach A, Pannicke T (2008) Neuroscience. A new glance at glia. Science 322:693–694

    Article  CAS  PubMed  Google Scholar 

  120. Ringstad N, Abe N, Horvitz HR (2009) Ligand-gated chloride channels are receptors for biogenic amines in C. elegans. Science 325:96–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Rival T, Soustelle L, Strambi C, Besson MT, Iche M, Birman S (2004) Decreasing glutamate buffering capacity triggers oxidative stress and neuropil degeneration in the Drosophila brain. Curr Biol 14:599–605

    Article  CAS  PubMed  Google Scholar 

  122. Roots BI, Lane NJ (1983) Myelinating glia of earthworm giant axons: thermally induced intramembranous changes. Tissue Cell 15:695–709

    Article  CAS  PubMed  Google Scholar 

  123. Ryan TJ, Grant SG (2009) The origin and evolution of synapses. Nat Rev Neurosci 10:701–712

    Article  CAS  PubMed  Google Scholar 

  124. Saubermann AJ, Castiglia CM, Foster MC (1992) Preferential uptake of rubidium from extracellular space by glial cells compared to neurons in leech ganglia. Brain Res 577:64–72

    Article  CAS  PubMed  Google Scholar 

  125. Schikorski D, Cuvillier-Hot V, Leippe M, Boidin-Wichlacz C, Slomianny C, Macagno E, Salzet M, Tasiemski A (2008) Microbial challenge promotes the regenerative process of the injured central nervous system of the medicinal leech by inducing the synthesis of antimicrobial peptides in neurons and microglia. J Immunol 181:1083–1095

    Article  CAS  PubMed  Google Scholar 

  126. Schwabe T, Bainton RJ, Fetter RD, Heberlein U, Gaul U (2005) GPCR signaling is required for blood-brain barrier formation in drosophila. Cell 123:133–144

    Article  CAS  PubMed  Google Scholar 

  127. Seal RP, Daniels GM, Wolfgang WJ, Forte MA, Amara SG (1998) Identification and characterization of a cDNA encoding a neuronal glutamate transporter from Drosophila melanogaster. Recept Channels 6:51–64

    CAS  PubMed  Google Scholar 

  128. Sousa-Nunes R, Yee LL, Gould AP (2011) Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila. Nature 471:508–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Speder P, Liu J, Brand AH (2011) Nutrient control of neural stem cells. Curr Opin Cell Biol 23:724–729

    Article  CAS  PubMed  Google Scholar 

  130. Stenesen D, Moehlman AT, Kramer H (2015) The carcinine transporter CarT is required in Drosophila photoreceptor neurons to sustain histamine recycling. Elife 4:e10972

    Article  PubMed  PubMed Central  Google Scholar 

  131. Stork T, Bernardos R, Freeman MR (2012) Analysis of glial cell development and function in Drosophila. Cold Spring Harb Protoc 2012:1–17

    Article  PubMed  PubMed Central  Google Scholar 

  132. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, Klambt C (2008) Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28:587–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Stout RF Jr, Parpura V (2011) Voltage-gated calcium channel types in cultured C. elegans CEPsh glial cells. Cell Calcium 50:98–108

    Article  CAS  PubMed  Google Scholar 

  134. Stout RF Jr, Verkhratsky A, Parpura V (2014) Caenorhabditis elegans glia modulate neuronal activity and behavior. Front Cell Neurosci 8:67

    Article  PubMed  CAS  Google Scholar 

  135. Sukhdeo SC, Sukhdeo MVK (1994) Mesehnchyme cells in Fasciola hepatica (Platyhelmintes): Primive glia? Tissue Cell 26:123–131

    Article  CAS  PubMed  Google Scholar 

  136. Sukhdeo SC, Sukhdeo MVK, Mettrick DF (1988) Neurocytology of the cerebral ganglion of Fasciola hepatica (Platyhelminthes). J Comp Neurol 278:337–343

    Article  CAS  PubMed  Google Scholar 

  137. Tasdemir-Yilmaz OE, Freeman MR (2014) Astrocytes engage unique molecular programs to engulf pruned neuronal debris from distinct subsets of neurons. Genes Dev 28:20–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Thomas JH (1994) The mind of a worm. Science 264:1698–1699

    Article  CAS  PubMed  Google Scholar 

  139. Threadgold LT, Arme C (1974) Electron microscope studies of Fasciola hepatica. Expr Parasitol 35:389–405

    Article  CAS  Google Scholar 

  140. True JR, Yeh SD, Hovemann BT, Kemme T, Meinertzhagen IA, Edwards TN, Liou SR, Han Q, Li J (2005) Drosophila tan encodes a novel hydrolase required in pigmentation and vision. PLoS Genet 1:e63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  141. Tsacopoulos M, Veuthey AL, Saravelos SG, Perrottet P, Tsoupras G (1994) Glial cells transform glucose to alanine, which fuels the neurons in the honeybee retina. J Neurosci 14:1339–1351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Van Roy P, Briggs DE (2011) A giant Ordovician anomalocaridid. Nature 473:510–513

    Article  PubMed  CAS  Google Scholar 

  143. Verkhratsky A, Butt AM (2013) Glial physiology and pathophysiology. Wiley-Blackwell, Chichester

    Book  Google Scholar 

  144. Verkhratsky A, Nedergaard M (2018) Physiology of astroglia. Physiol Rev 98:239–389

    Article  CAS  PubMed  Google Scholar 

  145. Viehweger E, Robitail S, Rohon MA, Jacquemier M, Jouve JL, Bollini G, Simeoni MC (2008) Measuring quality of life in cerebral palsy children. Ann Readapt Med Phys 51:119–137

    Article  CAS  PubMed  Google Scholar 

  146. Wadsworth WG, Bhatt H, Hedgecock EM (1996) Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16:35–46

    Article  CAS  PubMed  Google Scholar 

  147. Ward S, Thomson N, White JG, Brenner S (1975) Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J Comp Neurol 160:313–337

    Article  CAS  PubMed  Google Scholar 

  148. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1–340

    Article  CAS  PubMed  Google Scholar 

  149. Wuttke WA, Pentreath VW (1990) Evidence for the uptake of neuronally derived choline by glial cells in the leech central nervous system. J Physiol 420:387–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Xiong WC, Montell C (1995) Defective glia induce neuronal apoptosis in the repo visual system of Drosophila. Neuron 14:581–590

    Article  CAS  PubMed  Google Scholar 

  151. Xiong WC, Okano H, Patel NH, Blendy JA, Montell C (1994) repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev 8:981–994

    Article  CAS  PubMed  Google Scholar 

  152. Xu K, Terakawa S (1993) Saltatory conduction and a novel type of excitable fenestra in shrimp myelinated nerve fibers. Jpn J Physiol 43(Suppl 1):S285–293

    PubMed  Google Scholar 

  153. Xu K, Terakawa S (1999) Fenestration nodes and the wide submyelinic space form the basis for the unusually fast impulse conduction of shrimp myelinated axons. J Exp Biol 202:1979–1989

    CAS  PubMed  Google Scholar 

  154. Yoshimura S, Murray JI, Lu Y, Waterston RH, Shaham S (2008) mls-2 and vab-3 Control glia development, hlh-17/Olig expression and glia-dependent neurite extension in C. elegans. Development 135:2263–2275

    Article  CAS  PubMed  Google Scholar 

  155. Zalc B, Goujet D, Colman D (2008) The origin of the myelination program in vertebrates. Curr Biol 18:R511–512

    Article  CAS  PubMed  Google Scholar 

  156. Zhang YV, Ormerod KG & Littleton JT. (2017). Astrocyte Ca2+ Influx Negatively Regulates Neuronal Activity. eNeuro 4

    Google Scholar 

  157. Ziegler AB, Brusselbach F, Hovemann BT (2013) Activity and coexpression of Drosophila black with ebony in fly optic lobes reveals putative cooperative tasks in vision that evade electroretinographic detection. J Comp Neurol 521:1207–1224

    Article  CAS  PubMed  Google Scholar 

  158. Zoran MJ, Drewes CD, Fourtner CR, Siegel AJ (1988) The lateral giant fibers of the tubificid worm, Branchiura sowerbyi: structural and functional asymmetry in a paired interneuronal system. J Comp Neurol 275:76–86

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

VP’s work is supported by a grant from the National Institute of General Medical Sciences of the National Institutes of Health (R01GM123971). VP is an Honorary Professor at University of Rijeka, Croatia.

Author information

Authors and Affiliations

  1. Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, M13 9PT, UK

    Alexei Verkhratsky

  2. Faculty of Health and Medical Sciences, Center for Basic and Translational Neuroscience, University of Copenhagen, 2200, Copenhagen, Denmark

    Alexei Verkhratsky

  3. Achucarro Center for Neuroscience, IKERBASQUE, Basque Foundation for Science, 48011, Bilbao, Spain

    Alexei Verkhratsky

  4. School of Life Science and Technology, Shanghai Tech University, #230 Haike Road, Shanghai, 201210, China

    Margaret S. Ho

  5. Department of Neurobiology, The University of Alabama at Birmingham, Birmingham, AL, USA

    Vladimir Parpura

  6. University of Rijeka, Rijeka, Croatia

    Vladimir Parpura

Authors
  1. Alexei Verkhratsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Margaret S. Ho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vladimir Parpura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexei Verkhratsky .

Editor information

Editors and Affiliations

  1. Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, UK

    Alexei Verkhratsky

  2. School of Life Science and Technology, ShanghaiTech University, Shanghai, China

    Margaret S. Ho

  3. Institute of Pathophysiology, University of Ljubljana, Ljubljana, Slovenia

    Robert Zorec

  4. Department of Neurobiology, The University of Alabama at Birmingham, Birmingham, AL, USA

    Vladimir Parpura

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Verkhratsky, A., Ho, M.S., Parpura, V. (2019). Evolution of Neuroglia. In: Verkhratsky, A., Ho, M., Zorec, R., Parpura, V. (eds) Neuroglia in Neurodegenerative Diseases. Advances in Experimental Medicine and Biology, vol 1175. Springer, Singapore. https://doi.org/10.1007/978-981-13-9913-8_2

Download citation

Publish with us

Policies and ethics

Search

Navigation