Cell proliferation in the central nervous system of an adult semiterrestrial crab

Abstract

Neurogenesis occurs in adults of most organisms, both vertebrates and invertebrates. In semiterrestrial crabs of the infraorder Brachyura, the deutocerebrum, where neurogenesis occurs, processes the olfactory sensory information from the antennae. The deutocerebrum is composed of a pair of olfactory lobes associated with cell clusters 9 and 10 (Cl 9 and Cl 10), containing proliferating cells. Because the location of the neurogenic niche in brachyuran semiterrestrial crabs has not been defined, here we describe a neurogenic niche in the central olfactory system of the crab Ucides cordatus and report two types of glial cells in the deutocerebrum, based on different markers. Serotonin (5-hydroxytryptamine) labeling was used to reveal neuroanatomical aspects of the central olfactory system and the neurogenic niche. The results showed a zone of proliferating neural cells within Cl 10, which also contains III beta-tubulin (Tuj1)+ immature neurons, associated with a structure that has characteristics of the neurogenic niche. For the first time, using two glial markers, glial fibrillary acidic protein (GFAP) and glutamine synthetase (GS), we identified two types of astrocyte-like cells in different regions of the deutocerebrum. This study adds to the understanding of neurogenesis in a brachyuran semiterrestrial crustacean and encourages comparative studies between crustaceans and vertebrates, including mammals, based on shared aspects of both mechanisms of neurogenesis and regenerative potentials.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Abbreviations

AL:

Accessory lobe

BrdU:

5-Bromo-2′-deoxyuridine

Cl 9:

Cluster 9

Cl 10:

Cluster 10

DAPi:

4′,6-Diamidino-2-phenylindole

DGN:

Dorsal-giant neurons

EM:

External medulla

GFAP:

Glial fibrillary acidic protein

GS:

Glutamine synthetase

HB:

Hemiellipsoid body

IM:

Internal medulla

5HT:

5-Hydroxytryptamine (serotonin)

L:

Lamina

NeuN:

Neuronal nuclei

OGT:

Olfactory globular tract

OL:

Olfactory lobe

ORNs:

Olfactory receptor neurons

PBS:

Phosphate buffer saline

PH3:

Phospho-histone H3

PF:

Paraformaldehyde

PI:

Propidium iodide

TM:

Terminal medulla

Tuj1:

III beta-tubulin

References

  1. Allodi S, Da Silva SF, Taffarel M (1999) Glial cells of the central nervous system in the crab Ucides cordatus. Invert Biol 118:175–183

    Article  Google Scholar 

  2. Allodi S, Bressan CM, Carvalho SL, Cavalcante LA (2006) Regionally specific distribution of the binding of anti-glutamine synthetase and anti-S100 antibodies and of Datura stramonium lectin in glial domains of the optic lobe of the giant prawn. Glia 53:612–620

    PubMed  Article  Google Scholar 

  3. Altman J, Das GD (1967) Postnatal neurogenesis in the guinea-pig. Nature 214:1098–1101

    CAS  PubMed  Article  Google Scholar 

  4. Anlauf E, Derouiche A (2013) Glutamine synthetase as an astrocytic marker: its cell type and vesicle localization. Front Endocrinol 4:144

    Article  Google Scholar 

  5. Araújo MSLC, Calado TCS (2008) Bioecologia do caranguejo-uçá Ucides cordatus (Linnaeus) no Complexo Estuarino Lagunar Mundaú/Manguaba (CELMM), Alagoas. Brasil Revista da Gestão Costeira Integrada 8(2):169–181

    Article  Google Scholar 

  6. Augusto-Oliveira M, Arrifano GPF, Malva JO, Crespo-Lopez ME (2019) Adult hippocampal neurogenesis in different taxonomic groups: possible functional similarities and striking controversies. Cells 8:125

    PubMed Central  Article  PubMed  Google Scholar 

  7. Barker JM, Boonstra R, Wojtowicz JM (2011) From pattern to purpose: how comparative studies contribute to understanding the function of adult neurogenesis. Eur J Neurosci 34:963–977

    PubMed  Article  Google Scholar 

  8. Bazin F (1969) Étude comparée d’un organe deutocérébral chez les Crustacés Décapodes Reptantia. Comptes Rendus de l’Académie des Sciences 269:958–961

    Google Scholar 

  9. Beltz BS, Benton JL (2017) From blood to brain: adult-born neurons in the crayfish brain are the progeny of cells generated by the immune system. Front Neurosci 11:662–677

    PubMed  PubMed Central  Article  Google Scholar 

  10. Benton JL, Zhang Y, Kirkhart CR, Sandeman DC, Beltz BS (2011) Primary neuronal precursors in adult crayfish brain: replenishment from a non-neuronal source. BMC Neurosci 12:53

    PubMed  PubMed Central  Article  Google Scholar 

  11. Benton JL, Kery R, Li J, Noonin C, Söderhäll I, Beltz BS (2014) Cells from the immune system generate adult-born neurons in crayfish. Dev Cell 30:322–333

    CAS  PubMed  Article  Google Scholar 

  12. Brenneis G, Beltz BS (2019) Adult neurogenesis in crayfish: origin, expansion and migration of neural progenitor lineages in a pseudostratified neuroepithelium. J Comp Neurol 528(9):1459–1485

    PubMed  Article  Google Scholar 

  13. Cayre M, Malaterre J, Scotto-Lomassese S, Strambi C, Strambi A (2002) The common properties of neurogenesis in the adult brain: from invertebrates to vertebrates. Comp Biochem Physiol B 132:1–15

    PubMed  Article  Google Scholar 

  14. Chaves da Silva PG, Benton JL, Beltz BS, Allodi S (2012) Adult neurogenesis: ultrastructure of a neurogenic niche and neurovascular relationships. PLoS One 7(6):e39267

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  15. Da Silva SF, Allodi S (2000) A comparative study of neurons and glial cells in the lamina ganglionaris of two crustaceans. Braz J Morphol Sci 17:31–34

    Google Scholar 

  16. Da Silva SF, Taffarel M, Allodi S (2001) Crustacean visual system: an investigation on glial cells and their relation to extracellular matrix. Biol Cell 93:293–299

    Article  Google Scholar 

  17. Da Silva SF, Bressan CM, Cavalcante LA, Allodi S (2003) Binding of an antibody against a non-compact myelin protein to presumptive glial cells in the visual system of the crab Ucides cordatus. Glia 43:292–298

    PubMed  Article  Google Scholar 

  18. Da Silva SF, Correa CL, Tortelote GG, Einckert-Lamas M, Martinez AM, Allodi S (2004) Glial fibrillary acidic protein (GFAP)-like immunoreactivity in the visual system of the crab Ucides cordatus (Crustacea, Decapoda). Biol Cell 96:727–734

    Article  CAS  Google Scholar 

  19. Hansen A, Schmidt M (2001) Neurogenesis in the central olfactory pathway of the adult shore crab Carcinus maenas is controlled by sensory afferents. J Comp Neurol 441:223–233

    CAS  PubMed  Article  Google Scholar 

  20. Harzsch S (2003) Ontogeny of the ventral nerve cord in malacostracan crustaceans: a common plan for neuronal development in Crustacea, Hexapoda and other Arthropoda? Arthropod Struct Dev 32:17–37

    PubMed  Article  Google Scholar 

  21. Harzsch S, Benton J, Dawirs RR, Beltz B (1999) A new look at embryonic development of the visual system in decapod crustaceans: neuropil formation, neurogenesis, and apoptotic cell death. J Neurobiol 39:294–306

    CAS  PubMed  Article  Google Scholar 

  22. Hartline DK (2011) The evolutionary origins of glia. Glia 59:1215–1236

    PubMed  Article  Google Scholar 

  23. Hollmann G, Fonseca DB, Allodi S, Nery LEM (2011) Effects of seasonality and moult cycle on the proliferation of nerve cells and on the labelling of ecdysone receptors in an estuarine crab. J Comp Physiol A 13:359–367

    Google Scholar 

  24. Hollmann G, Ferreira GJ, Geihs MA, Vargas MA, Nery LEM, Linden R, Allodi S (2015) Antioxidant activity stimulated by ultraviolet radiation in the nervous system of a crustacean. Aquatic Toxicol 160:151–162

    CAS  Article  Google Scholar 

  25. Hollmann G, Linden R, Giangrande A, Allodi S (2016) Increased p53 and decreased p21 accompany apoptosis induced by ultraviolet radiation in the nervous system of a crustacean. Aquatic Toxicol 173:1–8

    CAS  Article  Google Scholar 

  26. Kempermann G (2012) New neurons for “survival of the fittest.” Nat Rev Neurosci 13:727–736

    CAS  PubMed  Article  Google Scholar 

  27. Kempermann G (2016) Adult neurogenesis: an evolutionary perspective. Cold Spring Harb Perspect Biol 8:a018986

    PubMed Central  Article  PubMed  Google Scholar 

  28. Kimble M, Dettman RW, Raff EC (1990) The -3-tubulin gene of Drosophila melanogaster is essential for viability and fertility. Genetics 126:991–1005

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. Krieger J, Braun P, Rivera NT, Schubart CD, Müller CHG, Harzsch S (2015) Comparative analyses of olfactory systems in terrestrial crabs (Brachyura): evidence for aerial olfaction? PeerJ 3:e1433

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  30. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    CAS  Article  Google Scholar 

  31. Lindsey BW, Tropepe V (2006) A comparative framework for understanding the biological principles of adult neurogenesis. Prog Neurobiol 80:281–307

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  32. Linser PJ, Trapido-Rosenthal HG, Orona E (1997) Glutamine synthetase is a glial-specific marker in the olfactory regions of the lobster Panulirus argus nervous system. Glia 20:275–283

    CAS  PubMed  Article  Google Scholar 

  33. Mead KS (2009) Do antennule and aesthetasc structure in the crayfish Orconectes virilis correlate with flow habitat? Integr Comp Biol 48:823–833

    Article  Google Scholar 

  34. Medina BNSP, Abreu IS, Cavalcante LA, Silva WAB, Fonseca RN, Allodi S, Barros CM (2015) 3-acetylpyridine-induced degeneration in the adult ascidian neural complex: Reactive and regenerative changes in glia and blood cells. Dev Neurobiol 75(8):877–893

    CAS  PubMed  Article  Google Scholar 

  35. Ortega A, Olivares-Bañuelos TN (2020) Neurons and glia cells in marine invertebrates: an update. Front Neurosci 14:121–135

    PubMed  PubMed Central  Article  Google Scholar 

  36. Pentreath VW (1987) Functions of invertebrate glia, in Nervous Systems in Invertebrates (Ali MA, ed.), NATO ASI Series A, vol. 141, Plenum, New York and London, pp. 61–103.

  37. Radojcic T, Pentreath VW (1979) Invertebrate glia. Prog Neurobiol 12:115–179

    CAS  PubMed  Article  Google Scholar 

  38. Sandeman DC, Sandeman RE, Aitken AR (1988) Atlas of serotonin containing neurons in the optic lobes and brain of the crayfish Cherax destructor. J Comp Neurol 269:465–478

    CAS  PubMed  Article  Google Scholar 

  39. Sandeman D, Sandeman R, Derby C, Schmidt M (1992) Morphology of the brain of crayfish, crabs, and spiny lobster: a common nomenclature for homologous structures. Biol Bull 183:304–326

    CAS  PubMed  Article  Google Scholar 

  40. Sandeman DC, Beltz BS, Sandeman R (1995) Crayfish brain interneurons that converge with serotonin giant cells in accessory lobe glomeruli. J Comp Neurol 352:263–279

    CAS  PubMed  Article  Google Scholar 

  41. Sandeman DC, Scholtz G (1995) Ground plans, evolutionary changes and homologies in decapod crustacean brains. In: Kutsch W, Breidbach O (eds) The nervous systems of invertebrates: a comparative approach. Birkhäuser, Basel, pp 329–348

    Google Scholar 

  42. Sandeman DC, Benton JL, Beltz BS (2009) An identified serotonergic neuron regulates adult neurogenesis in the crustacean brain. Develop Neurobiol 69:530–545

    CAS  Article  Google Scholar 

  43. Sandeman DC, Bazin B, Beltz BS (2011) Adult neurogenesis: examples from the decapod crustaceans and comparisons with mammals. Arthropod Struct Dev 40:258–275

    PubMed  PubMed Central  Article  Google Scholar 

  44. Sandeman DC, Kenning M, Harzsch S (2014) Adaptive trends in malacostracan brain form and function related to behavior. In: Derby C, Thiel M (eds) Crustacean nervous system and their control of behaviour. The natural history of the Crustacea, vol. 3. Oxford: Oxford University Press, pp 11–48

  45. Sandeman R, Clarke D, Sandeman DC, Manly M (1998) Growth-related and antennular amputation-induced changes in the olfactory centers of crayfish brain. J Neurosci 18:6195–6206

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. Schmidt M (1997) Continuous neurogenesis in the olfactory brain of adult shore crabs, Carcinus maenas. Brain Res 762:131–143

    CAS  PubMed  Article  Google Scholar 

  47. Schmidt M (2001) Neuronal differentiation and long-term survival of newly generated cells in the olfactory midbrain of the adult spiny lobster, Panulirus argus. J Neurobiol 48:181–203

    CAS  PubMed  Article  Google Scholar 

  48. Schmidt M, Ache BW (1997) Immunocytochemical analysis of glomerular regionalization and neuronal diversity in the olfactory deutocerebrum of the spiny lobster. Cell Tissue Res 287:541563

    Article  Google Scholar 

  49. Schmidt M, Derby CD (2011) Cytoarchitecture and ultrastructure of neural stem cell niches and neurogenic complexes maintaining adult neurogenesis in the olfactory midbrain of spiny lobsters Panulirus argus. J Comp Neurol 519:2283–2319

    PubMed  Article  Google Scholar 

  50. Schmidt M, Harzsch S (1999) Comparative analysis of neurogenesis in the central olfactory pathway of adult decapod crustaceans by in vivo BrdU labeling. Biol Bull 196:127–136

    CAS  PubMed  Article  Google Scholar 

  51. Song CK, Johnstone LM, Edwards DH, Derby CD, Schmid M (2009) Cellular basis of neurogenesis in the brain of crayfish, Procambarus clarkii: neurogenic complex in the olfactory midbrain from hatchlings to adults. Arthropod Struct Dev 38:339–360

    CAS  PubMed  Article  Google Scholar 

  52. Sullivan J, Beltz B (2001) Neural pathways connecting the deutocerebrum and lateral protocerebrum in the brains of decapod crustaceans. J Comp Neurol 441:9–22

    CAS  PubMed  Article  Google Scholar 

  53. Sullivan JM, Beltz BS (2005) Newborn cells in the adult crayfish brain differentiate into distinct neuronal types. J Neurobiol 65:157–170

    PubMed  Article  Google Scholar 

  54. Sullivan JM, Benton JL, Sandeman DC, Beltz BS (2007) Adult neurogenesis: a common strategy across diverse species. J Comp Neurol 500:574–584

    PubMed  PubMed Central  Article  Google Scholar 

  55. Wajsenzon IJR, De Carvalho LA, Biancalana A, Da Silva WAB, Dos Santos MCL, De Araujo EG, Allodi S (2016) Culture of neural cells of the eyestalk of a mangrove crab is optimized on poly-l-ornithine substrate. Cytotec 68:2193–2206

    CAS  Article  Google Scholar 

  56. Waldrop LD, Miller LA, Khatri S (2016) A tale of two antennules: the performance of crab odour-capture organs in air and water. J R Soc Interface 13:20160615

    PubMed  PubMed Central  Article  Google Scholar 

  57. Wittfoth C, Harzsch S (2018) Adult neurogenesis in the central olfactory pathway of dendrobranchiate and caridean shrimps: new insights into the evolution of the deutocerebral proliferative system in reptant decapods. Dev Neurobiol 78:757–774

    CAS  Article  Google Scholar 

  58. Zhang H, Yu P, Zhong S, Ge T, Peng S, Zhou Z, Guo X (2016) Gliocyte and synapse analyses in cerebral ganglia of the Chinese mitten crab Eriocheir sinensis: ultrastructural study. Europ J Histochem 60:2655

    CAS  Google Scholar 

Download references

Funding

This study was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Gabriela Hollmann.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All procedures adopted in this study, including the location where the animals were captured, were performed after approval by the National Environmental Committee (Certificate # 14689-1/IBAMA/2008, permission to use the animals # 2440408) and by the Ethics Commission on Research Animals of the Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro (protocol DHEICB 005). This article does not contain any studies with human participants performed by any of the authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (TIF 3641 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hollmann, G., da Silva, P.G.C., Linden, R. et al. Cell proliferation in the central nervous system of an adult semiterrestrial crab. Cell Tissue Res (2021). https://doi.org/10.1007/s00441-021-03413-y

Download citation

Keywords

  • Decapod crustacean
  • Neurogenesis
  • Olfactory lobe
  • Mangrove crab
  • Glial cell