Genoarchitecture of the rostral hindbrain of a shark: basis for understanding the emergence of the cerebellum at the agnathan–gnathostome transition
- 306 Downloads
The cerebellum is present in all extant gnathostomes or jawed vertebrates, of which cartilaginous fishes represent the most ancient radiation. Since the isthmic organizer induces the formation of the cerebellum, comparative genoarchitectonic analysis on the meso-isthmo-cerebellar region of cartilaginous fishes with respect to that of jawless vertebrates could reveal why the isthmic organizer acquires the ability to induce the formation of the cerebellum in gnathostomes. In the present work we analyzed the expression pattern of a variety of genes related to the cerebellar formation and patterning (ScOtx2, ScGbx2, ScFgf8, ScLmx1b, ScIrx1, ScIrx3, ScEn2, ScPax6 and ScLhx9) by in situ hybridization, and the distribution of Pax6 protein in the developing hindbrain of the shark Scyliorhinus canicula. The genoarchitectonic code in this species revealed high degree of conservation with respect to that of other gnathostomes. This resemblance may reveal the features of the ancestral condition of the gene network operating for specification of the rostral hindbrain patterning. Accordingly, the main subdivisions of the rostral hindbrain of S. canicula could be recognized. Our results support the existence of a rhombomere 0, identified as the ScFgf8/ScGbx2/ScEn2-positive and mainly negative ScIrx3 domain just caudal to the midbrain ScIrx1/ScOtx2/ScLmx1b-positive domain. The differential ScEn2 and Pax6 expression in the rhombomere 1 revealed anterior and posterior subdivisions. Interestingly, dissimilarities between S. canicula and lampreys (jawless vertebrates) were noted in the expression of Irx, Lhx and Pax genes, which could be part of significant gene network changes through evolution that caused the emergence of the cerebellum.
KeywordsChondrichthyan Neural genoarchitecture Isthmus Midbrain–hindbrain boundary Rhombomeres
We thank Prof. Dr. R. Anadón for the valuable comments made during the preparation of this paper and his critical reading of the manuscript. We also thank Dr. S. Ferreiro-Galve for her helpful support and contribution in some experimental procedures. This work was supported by grants from the Spanish Dirección General de Investigación-FEDER (BFU2010-15816), the Xunta de Galicia (10PXIB200051PR, CN 2012/237), and European Community-Research Infrastructure Action under the FP7 “Capacities” Specific Programme (ASSEMBLE 227799).
Conflict of interest
The authors declare that they have no conflict of interest
The manuscript does not contain clinical studies or patient data.
- Adachi N, Takechi M, Hirai T, Kuratani S (2012) Development of the head and trunk mesoderm in the dogfish, Scyliorhinus torazame: II. Comparison of gene expression between the head mesoderm and somites with reference to the origin of the vertebrate head. Evol Dev 14:257–276PubMedCrossRefGoogle Scholar
- Allen Developing Mouse Brain Atlas [Internet] (2009) Allen Institute for Brain Science, Seattle. http://developingmouse.brain-map.org
- Alonso A, Merchán P, Sandoval JE, Sánchez-Arrones L, Garcia-Cazorla A, Artuch R, Ferrán JL, Martínez-de-la-Torre M, Puelles L (2013) Development of the serotonergic cells in murine raphe nuclei and their relations with rhombomeric domains. Brain Struct Funct 218:1229–1277PubMedPubMedCentralCrossRefGoogle Scholar
- Compagnucci C, Debiais-Thibaud M, Coolen M, Fish J, Griffin JN, Bertocchini F, Minoux M, Rijli FM, Borday-Birraux V, Casane D, Mazan S, Depew MJ (2013) Pattern and polarity in the development and evolution of the gnathostome jaw: both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula. Dev Biol 377:428–448PubMedCrossRefGoogle Scholar
- Coolen M, Menuet A, Chassoux D, Compagnucci C, Henry S, Lévèque L, Da Silva C, Gavory F, Samain S, Wincker P, Thermes C, D’Aubenton-Carafa Y, Rodriguez-Moldes I, Naylor G, Depew M, Sourdaine P, Mazan S (2009) The dogfish Scyliorhinus canicula, a reference in jawed vertebrates. In: Behringer RR, Johnson AD, Krumlauf RE (eds) Emerging model organisms. A laboratory manual, vol 1. CSHL Press, Cold Spring Harbor, pp 431–446Google Scholar
- Lebel M, Agarwal P, Cheng CW, Kabir MG, Chan TY, Thanabalasingham V, Zhang X, Cohen DR, Husain M, Cheng SH, Bruneau BG, Hui CC (2003) The Iroquois homeobox gene Irx2 is not essential for normal development of the heart and midbrain–hindbrain boundary in mice. Mol Cell Biol 23:8216–8225PubMedPubMedCentralCrossRefGoogle Scholar
- Martínez S (2001) The isthmic organizer and brain regionalization. Int J Dev Biol 44:367–371Google Scholar
- Puelles L, Marín F, MartínezdelaTorre S, Martínez S (1995) The midbrain–hindbrain junction: a model system for brain regionalization through morphogenetic neuroepithelial interactions. In: Lonai P (ed) Towards analysis of vertebrate development. Harwood Publishers, Chur, pp 173–197Google Scholar
- Vaage S (1969) The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological histochemical and autoradiographic investigation. In: Brodal HOH et al (eds) Advances in anatomy, embryology and cell biology. Springer, Berlin, pp 5–21Google Scholar
- Watson C, Paxinos G, Puelles L (2012) The mouse nervous system. Elsevier Academic Press, LondonGoogle Scholar