Skip to main content

Anteroposterior Regionalization of the Brain: Genetic and Comparative Aspects

  • Chapter
Brain Development in Drosophila melanogaster

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 628))

Abstract

Developmental genetic analyses of embryonic CNS development in Drosophila have uncovered the role of key, high-order developmental control genes in anteroposterior regionalization of the brain. The gene families that have been characterized include the otd/Otx and ems/Emx genes which are involved in specification of the anterior brain, the Hox genes which are involved in the differentiation of the posterior brain and the Pax genes which are involved in the development of the anterior/posterior brain boundary zone. Taken together with work on the genetic control of mammalian CNS development, these findings indicate that all three gene sets have evolutionarily conserved roles in brain development, revealing a surprising evolutionary conservation in the molecular mechanisms of brain regionalization.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arendt D, Nubler-Jung K. Comparison of early nerve cord development in insects and vertebrates. Development 1999; 126(11):2309–2325.

    PubMed  CAS  Google Scholar 

  2. Reichert H, Simeone A. Conserved usage of gap and homeotic genes in patterning the CNS. Curr Opin Neurobiol 1999; 9(5):589–595.

    Article  PubMed  CAS  Google Scholar 

  3. Adoutte A, Balavoine G, Lartillot N et al. The new animal phylogeny: reliability and implications. Proc Natl Acad Sci USA 2000; 97(9):4453–4456.

    Article  PubMed  CAS  Google Scholar 

  4. Younossi-Hartenstein A, Nassif C, Green P et al. Early neurogenesis of the Drosophila brain. J Comp Neurol 1996; 370(3):313–329.

    Article  PubMed  CAS  Google Scholar 

  5. Lumsden A, Krumlauf R. Patterning the vertebrate neuraxis. Science 1996; 274(5290):1109–1115.

    Article  PubMed  CAS  Google Scholar 

  6. Puelles L, Rubenstein JL. Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 2003; 26(9):469–476.

    Article  PubMed  CAS  Google Scholar 

  7. Dalton D, Chadwick R, McGinnis W. Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev 1989; 3(12A):1940–1956.

    Article  PubMed  CAS  Google Scholar 

  8. Finkelstein R, Perrimon N. The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 1990; 346(6283):485–488.

    Article  PubMed  CAS  Google Scholar 

  9. Walldorf U, Gehring WJ. Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J 1992; 11(6):2247–2259.

    PubMed  CAS  Google Scholar 

  10. Cohen SM, Jurgens G. Mediation of Drosophila head development by gap-like segmentation genes. Nature 1990; 346(6283):482–485.

    Article  PubMed  CAS  Google Scholar 

  11. Schmidt-Ott U, Gonzalez-Gaitan M, Jackie H et al. Number, identity and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants. Proc Natl Acad Sci USA 1994; 91(18):8363–8367.

    Article  PubMed  CAS  Google Scholar 

  12. Urbach R, Technau GM. Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 2003; 130(16):3621–3637.

    Article  PubMed  CAS  Google Scholar 

  13. Younossi-Hartenstein A, Green P, Liaw GJ et al. Control of early neurogenesis of the Drosophila brain by the head gap genes tll, otd, ems and btd. Dev Biol 1997; 182(2):270–283.

    Article  PubMed  CAS  Google Scholar 

  14. Hirth F, Therianos S, Loop T et al. Developmental defects in brain segmentation caused by mutations of the homeobox genes orthodenticle and empty spiracles in Drosophila. Neuron 1995; 15(4):769–778.

    Article  PubMed  CAS  Google Scholar 

  15. Hartmann B, Hirth F, Walldorf U et al. Expression, regulation and function of the homeobox gene empty spiracles in brain and ventral nerve cord development of Drosophila. Mech Dev 2000; 90(2):143–153.

    Article  PubMed  CAS  Google Scholar 

  16. Leuzinger S, Hirth F, Gerlich D et al. Equivalence of the fly orthodenticle gene and the human OTX genes in embryonic brain development of Drosophila. Development 1998; 125(9):1703–1710.

    PubMed  CAS  Google Scholar 

  17. Acampora D, Annino A, Tuorto F et al. Otx genes in the evolution of the vertebrate brain. Brain Res Bull 2005; 66(4–6):410–420.

    Article  PubMed  CAS  Google Scholar 

  18. Cecchi C. Emx:2 a gene responsible for cortical development, regionalization and area specification. Gene 2002; 291(1–2):1–9.

    Article  PubMed  CAS  Google Scholar 

  19. Simeone A, Acampora D, Gulisano M et al. Nested expression domains of four homeobox genes in developing rostral brain. Nature 1992; 358(6388):687–690.

    Article  PubMed  CAS  Google Scholar 

  20. Acampora D, Mazan S, Avantaggiato V et al. Epilepsy and brain abnormalities in mice lacking the Otxl gene. Nat Genet 1996; 14(2):218–222.

    Article  PubMed  CAS  Google Scholar 

  21. Acampora D, Mazan S, Lallemand Y et al. Forebrain and midbrain regions are deleted in Otx2-/-mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 1995; 121(10):3279–3290.

    PubMed  CAS  Google Scholar 

  22. Acampora D, Avantaggiato V, Tuorto F et al. Murine Otxl and Drosophila otd genes share conserved genetic functions required in invertebrate and vertebrate brain development. Development 1998; 125(9):1691–1702.

    PubMed  CAS  Google Scholar 

  23. Acampora D, Boyl PP, Signore M et al. OTD/OTX2 functional equivalence depends on 5′ and 3′ UTR-mediated control of Otx2 mRNA for nucleo-cytoplasmic export and epiblast-restricted translation. Development 2001; 128(23):4801–4813.

    PubMed  CAS  Google Scholar 

  24. Simeone A, Gulisano M, Acampora D et al. Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. EMBO J 1992; 11(7):2541–2550.

    PubMed  CAS  Google Scholar 

  25. Gulisano M, Broccoli V, Pardini C et al. Emxl and Emx2 show different patterns of expression during proliferation and differentiation of the developing cerebral cortex in the mouse. Eur J Neurosci 1996; 8(5):1037–1050.

    Article  PubMed  CAS  Google Scholar 

  26. Bishop KM, Rubenstein JL, O’Leary DD. Distinct actions of Emxl, Emx2 and Pax6 in regulating the specification of areas in the developing neocortex. J Neurosci 1 2002; 22(17):7627–7638.

    PubMed  CAS  Google Scholar 

  27. Muzio L, DiBenedetto B, Stoykova A et al. Conversion of cerebral cortex into basal ganglia in Emx2(-/-) Pax6(Sey/Sey) double-mutant mice. Nat Neurosci 2002; 5(8):737–745.

    PubMed  CAS  Google Scholar 

  28. Qiu M, Anderson S, Chen S et al. Mutation of the Emx-1 homeobox gene disrupts the corpus callosum. Dev Biol 1996; 178(1):174–178.

    Article  PubMed  CAS  Google Scholar 

  29. Yoshida M, Suda Y, Matsuo I et al. Emxl and Emx2 functions in development of dorsal telencephalon. Development 1997; 124(1):101–111.

    PubMed  CAS  Google Scholar 

  30. Ferrier DE, Holland PW. Ancient origin of the Hox gene cluster. Nat Rev Genet 2001; 2(1):33–38.

    Article  PubMed  CAS  Google Scholar 

  31. Hughes CL, Kaufman TC. Hox genes and the evolution of the arthropod body plan. Evol Dev 2002; 4(6):459–499.

    Article  PubMed  CAS  Google Scholar 

  32. Mann RS. Why are Hox genes clustered? Bioessays 1997; 19(8):661–664.

    Article  PubMed  CAS  Google Scholar 

  33. Duboule D, Morata G. Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet 1994; 10(10):358–364.

    Article  PubMed  CAS  Google Scholar 

  34. Hirth F, Hartmann B, Reichert H. Homeotic gene action in embryonic brain development of Drosophila. Development 1998; 125(9):1579–1589.

    PubMed  CAS  Google Scholar 

  35. Kourakis MJ, Master VA, Lokhorst DK et al. Conserved anterior boundaries of Hox gene expression in the central nervous system of the leech Helobdella. Dev Biol 1997; 190(2):284–300.

    Article  PubMed  CAS  Google Scholar 

  36. Lowe CJ, Wu M, Salic A et al. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 2003; 113(7):853–865.

    Article  PubMed  CAS  Google Scholar 

  37. Wilkinson DG, Bhatt S, Cook M et al. Segmental expression of Hox-2 homoeobox-containing genes in the developing mouse hindbrain. Nature 1989; 341(6241):405–409.

    Article  PubMed  CAS  Google Scholar 

  38. Hunt P, Krumlauf R. Deciphering the Hox code: clues to patterning branchial regions of the head. Cell 1991; 66(6):1075–1078.

    Article  PubMed  CAS  Google Scholar 

  39. Gavalas A, Studer M, Lumsden A et al. Hoxal and Hoxbl synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 1998; 125(6):1123–1136.

    PubMed  CAS  Google Scholar 

  40. Studer M, Lumsden A, Ariza-McNaughton L et al. Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 1996; 384(6610):630–634.

    Article  PubMed  CAS  Google Scholar 

  41. Bruce AE, Shankland M. Expression of the head gene Lox22-Otx in the leech Helobdella and the origin of the bilaterian body plan. Dev Biol 1998; 201(1):101–112.

    Article  PubMed  CAS  Google Scholar 

  42. Canestro C, Bassham S, Postlethwait J. Development of the central nervous system in the larvacean Oikopleura dioica and the evolution of the chordate brain. Dev Biol 2005; 285(2):298–315.

    Article  PubMed  CAS  Google Scholar 

  43. Castro LF, Rasmussen SL, Holland PW et al. A Gbx homeobox gene in amphioxus: Insights into ancestry of the ANTP class and evolution of the midbrain/hindbrain boundary. Dev Biol 2006.

    Google Scholar 

  44. Hirth F, Kammermeier L, Frei E et al. An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila. Development 2003; 130(11):2365–2373.

    Article  PubMed  CAS  Google Scholar 

  45. Liu A, Joyner AL. Early anterior/posterior patterning of the midbrain and cerebellum. Annu Rev Neurosci 2001; 24:869–896.

    Article  PubMed  CAS  Google Scholar 

  46. Wada H, Saiga H, Satoh N et al. Tripartite organization of the ancestral chordate brain and the antiquity of placodes: insights from ascidian Pax-2/5/8, Hox and Otx genes. Development 1998; 125(6):1113–1122.

    PubMed  CAS  Google Scholar 

  47. Wurst W, Bally-Cuif L. Neural plate patterning: upstream and downstream of the isthmic organizer. Nat Rev Neurosci 2001; 2(2):99–108.

    Article  PubMed  CAS  Google Scholar 

  48. Noll M. Evolution and role of Pax genes. Curr Opin Genet Dev 1993; 3(4):595–605.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Lichtneckert, R., Reichert, H. (2008). Anteroposterior Regionalization of the Brain: Genetic and Comparative Aspects. In: Technau, G.M. (eds) Brain Development in Drosophila melanogaster . Advances in Experimental Medicine and Biology, vol 628. Springer, New York, NY. https://doi.org/10.1007/978-0-387-78261-4_2

Download citation

Publish with us

Policies and ethics