Dynamic expression of Pax6 in the shark olfactory system: Evidence for the presence of pax6 cells along the olfactory nerve pathway

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution

Volumn 318, Issue 2, 2012, Pages 79-90

  Ferreiro Galve, Susana ^a   Candal, Eva ^a   Rodríguez Moldes, Isabel ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EYE PROTEIN; HOMEODOMAIN PROTEIN; PAIRED BOX TRANSCRIPTION FACTOR; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR PAX6;

ANIMAL; ARTICLE; DOGFISH; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; OLFACTORY NERVE; PHYSIOLOGY;

ANIMALS; DOGFISH; EYE PROTEINS; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; OLFACTORY NERVE; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS;

CHONDRICHTHYES; SCYLIORHINUS CANICULA; VERTEBRATA;

EID: 84860294153     PISSN: 15525007     EISSN: 15525015     Source Type: Journal    
DOI: 10.1002/jezmde.21444     Document Type: Article

References (68)

1. Abraham E, Palevitch O, Ijiri S, Du S-J, Gothilf Y, Zohar Y. 2008. Early development of forebrain gonadotropin-releasing hormone neurones and the role of GnRH as an autocrine migration factor. J Neuroendocrinol 20: 394-405.
2. Ballard WW, Mellinger J, Lechenault H. 1993. A series on normal stages for development of Scyliorhinus canicula, the lesser-spotted dogfish (Chondrichthyes: Scyliorhinidae). J Exp Zool (Mol Dev Evol) 267: 318-336.
3. Barraud P, Seferiadis AA, Tyson LD, Zwart MF, Szabo-Rogers HL, Ruhrberg C, Liu KJ, Baker CVH. 2010. Neural crest origin of olfactory ensheathing glia. PNAS 107: 21040-21045.
4. Behrens M, Venkatraman G, Gronostajski RM, Reed RR, Margolis FL. 2000. NFI in the development of the olfactory neuroepithelium and the regulation of olfactory marker protein gene expression. Eur J Neurosci 12: 1372-1384.
5. Blanchart A, Martín-López E, De Carlos JA, López-Mascaraque L. 2011. Peripheral contributions to olfactory bulb cell populations (migrations towards the olfactory bulb). Glia 59: 278-292.
6. Callaerts P, Halder G, Gehring WJ. 1997. Pax6 in development and evolution. Annu Rev Neurosci 20: 483-532.
7. Collinson JM, Quinn JC, Hill RE, West JD. 2003. The roles of Pax6 in the cornea, retina, and olfactory epithelium of the developing mouse embryo. Dev Biol 255: 303-312.
8. 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, Rodríguez-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, editors. Emerging model organisms. A laboratory manual, vol. 1. New York: Cold Spring Harbor. p 431-446.
9. Davis JA, Reed RR. 1996. Role of Olf-1 and Pax-6 transcription factors in neurodevelopment. J Neurosci 16: 5082-5094.
10. De Carlos JA, López-Mascaraque L, Valverde F. 1995. The telencephalic vesicles are innervated by olfactory placode-derived cells: a possible mechanism to induce neocortical development. Neuroscience 68: 1167-1178.
11. De Carlos JA, López-Mascaraque L, Valverde F. 1996. Early olfactory fiber projections and cell migration into the rat telencephalon. Int J Dev Neurosci 14: 853-866.
12. Dellovade TL, Pfaff DW, Schwanzel-Fukuda M. 1998. Olfactory bulb development is altered in small-eye (Sey) mice. J Comp Neurol 402: 402-418.
13. Demski LS, Fields RD. 1988. Dense-cored vesicle-containing components of the terminal nerve of sharks and rays. J Comp Neurol 278: 604-614.
14. Demski LS, Fields RD, Bullock TH, Schreibman MP, Margolis-Nunno H. 1987. The terminal nerve of sharks and rays: electron microscopic, immunocytochemical, and electrophysiological studies. Ann NY Acad Sci 519: 15-32.
15. Derobert Y, Baratte B, Lepage M, Mazan S. 2002. Pax6 expression patterns in Lampetra fluviatilis and Scyliorhinus canicula embryos suggest highly conserved roles in the early regionalization of the vertebrate brain. Brain Res Bull 57: 277-280.
16. Drapkin PT, Silverman AJ. 1999. Development of the chick olfactory nerve. Dev Dyn 214: 349-360.
17. Dryer L, Graziadei PP. 1993. A pilot study on morphological compartmentalization and heterogeneity in the elasmobranch olfactory bulb. Anat Embryol (Berl) 188: 41-51.
18. Dryer L, Graziadei PP. 1994a. Mitral cell dendrites: a comparative approach. Anat Embryol (Berl) 189: 91-106.
19. Dryer L, Graziadei PP. 1994b. Influence of the olfactory organ on brain development. Perspect Dev Neurobiol 2: 163-174.
20. Dryer L, Graziadei PP. 1996. Synaptology of the olfactory bulb of an elasmobranch fish, Sphyrna tiburo. Anat Embryol (Berl) 193: 101-114.
21. Ferrando S, Bottaro M, Gallus L, Girosi L, Vacchi M, Tagliafierro G. 2006a. Na1/K1ATPase immunoreactivity in olfactory epithelium of small-spotted catshark Scyliorhinus canicula (Linnaeus, 1758): possible presence of ion exchanging cells? J Fish Biol 69: 278-282.
22. Ferrando S, Bottaro M, Gallus L, Girosi L, Vacchi M, Tagliafierro G. 2006b. Observation of crypt neuron-like cells in the olfactory epithelium of a cartilaginous fish. Neurosci Lett 403: 280-282.
23. Ferrando S, Bottaro M, Gallus L, Girosi L, Vacchi M, Tagliafierro G. 2007a. First detection of olfactory marker protein (OMP) immunoreactivity in the olfactory epithelium of a cartilaginous fish. Neurosci Lett 413: 173-176.
24. Ferrando S, Bottaro M, Pedemonte F, De Lorenzo S, Gallus L, Tagliafierro G. 2007b. Appearance of crypt neurons in the olfactory epithelium of the skate Raja clavata during development. Anat Rec (Hoboken) 290: 1268-1272.
25. Ferrando S, Gambardella C, Ravera S, Bottero S, Ferrando T, Gallus L, Manno V, Salati AP, Ramoino P, Tagliafierro G. 2009. Immunolocalization of G-protein alpha subunits in the olfactory system of the cartilaginous fish Scyliorhinus canicula. Anat Rec (Hoboken) 292: 1771-1779.
26. Ferrando S, Gallus L, Gambardella C, Ghigliotti L, Ravera S, Vallarino M, Vacchi M, Tagliafierro G. 2010. Cell proliferation and apoptosis in the olfactory epithelium of the shark Scyliorhinus canicula. J Chem Neuroanat 40: 293-300.
27. Fishelson L, Baranes A. 1997. Ontogenesis and cytomorphology of the nasal olfactory organ in the oman shark, Iago omanensis (Triakidae), in the Gulf of Aqaba, Red Sea. Anat Rec 249: 409-421.
28. Forlano PM, Maruska KP, Sower SA, King JA, Tricas TC. 2000. Differential distribution of gonadotropin-releasing hormone-immunoreactive neurons in the stingray brain: functional and evolutionary considerations. Gen Comp Endocrinol 118: 226-248.
29. Fornaro M, Geuna S, Fasolo A, Giacobini-Robecchi MG. 2001. Evidence of very early neuronal migration from the olfactory placode of the chick embryo. Neuroscience 107: 191-197.
30. Fornaro M, Geuna S, Fasolo A, Giacobini-Robecchi MG. 2003. HuC/D confocal imaging points to olfactory migratory cells as the first cell population that expresses a post-mitotic neuronal phenotype in the chick embryo. Neuroscience 122: 123-128.
31. Forni PE, Taylor-Burds C, Melvin VS, Williams T, Wray S. 2011. Neural crest and ectodermal cells intermix in the nasal placode to give rise to GnRH-1 neurons, sensory neurons, and olfactory ensheathing cells. J Neurosci 31: 6915-6927.
32. Franco MD, Pape MP, Swiergiel JJ, Burd GD. 2001. Differential and overlapping expression patterns of X-dll3 and Pax-6 genes suggest distinct roles in olfactory system development of the African clawed frog Xenopus laevis. J Exp Biol 204: 2049-2061.
33. Franssen EHP, de Bree FM, Verhaagen J. 2007. Olfactory ensheathing glia: their contribution to primary olfactory nervous system regeneration and their regenerative potential following transplantation into the injured spinal cord. Brain Res Rev 56: 236-258.
34. Glardon S, Holland LZ, Gehring WJ, Holland ND. 1998. Isolation and developmental expression of the amphioxus Pax-6 gene (Amphi-Pax-6): insights into eye and photoreceptor evolution. Development 125: 2701-2710.
35. Grindley JC, Davidson DR, Hill RE. 1995. The role of Pax-6 in eye and nasal development. Development 121: 1433-1442.
36. Hill RE, Favor J, Hogan BLM, Ton CCT, Saunders GF, Hanson IM, Prosser J, Jordan T, Hastie ND, Heyningen V. 1991. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354: 522-525.
37. Hofmann MH, Northcutt RG. 2008. Organization of major telencephalic pathways in an elasmobranch, the thornback ray Platyrhinoidis triseriata. Brain Behav Evol 72: 307-325.
38. Hogan BLM, Horsburgh G, Cohen J, Hetherington CM, Fisher G, Lyon MF. 1986. Small eyes (Sey): a homozygous lethal mutation on chromosome 2 which affects the differentiation of both lens and nasal placodes in the mouse. J Embryol 97: 95-110.
39. Hsieh YW, Yang XJ. 2009. Dynamic Pax6 expression during the neurogenic cell cycle influences proliferation and cell fate choices of retinal progenitors. Neural Dev 4: 32-50.
40. Jiménez D, García C, de Castro F, Chedotal A, Sotelo C, de Carlos JA, Valverde F López-Mascaraque L. 2000. Evidence for intrinsic development of olfactory structures in Pax-6 mutant mice. J Comp Neurol 428: 511-526.
41. Kohwi M, Osumi N, Rubenstein JL, Alvarez-Buylla A. 2005. Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci 25: 6997-7003.
42. López-Mascaraque L, García C, Valverde F, de Carlos JA. 1998. Central olfactory structures in Pax-6 mutant mice. Ann NY Acad Sci 855: 83-94.
43. Maekawa M, Takashima N, Arai Y, Nomura T, Inokuchi K, Yuasa S, Osumi N. 2005. Pax6 is required for production and maintenance of progenitor cells in postnatal hippocampal neurogenesis. Genes Cells 10: 1001-1014.
44. Maier E, Gunhaga L. 2009. Dynamic expression of neurogenic markers in the developing chick olfactory epithelium. Dev Dyn 238: 1617-1625.
45. Maier E, Nord H, von Hofsten J, Gunhaga L. 2011. A balance of BMP and Notch activity regulates neurogenesis and olfactory nerve formation. PLoS ONE 6: e17379. DOI: 10.1371/journal.- pone.0017379.
46. Miller AM, Treloar HB, Greer CA. 2010. Composition of the migratory mass during development of the olfactory nerve. J Comp Neurol 518: 4825-4841.
47. Nomura T, Osumi N. 2004. Misrouting of mitral cell progenitors in the Pax6/small eye rat telencephalon. Development 131: 787-796.
48. Nomura T, Haba H, Osumi N. 2007. Role of a transcription factor Pax6 in the developing vertebrate olfactory system. Dev Growth Differ 49: 683-690.
49. Nural HF, Mastick GS. 2004. Pax6 guides a relay of pioneer longitudinal axons in the embryonic mouse forebrain. J Comp Neurol 479: 399-409.
50. O’Neill P, McCole RB, Baker CVH. 2007. A molecular analysis of neurogenic placode and cranial sensory ganglion development in the shark, Scyliorhinus canicula. Dev Biol 304: 156-181.
51. Osumi N, Shinoara H, Numayama-Tsuruta K, Maekawa M. 2008. Concise review: Pax6 transcription factor contributes to both embryonic and adult neurogenesis as a multifunctional regulator. Stem Cells 26: 1663-1672.
52. Palevitch O, Kight K, Abraham E, Wray S, Zohar Y, Gothilf Y. 2007. Ontogeny of the GnRH systems in zebrafish brain: in situ hybridization and promoter-reporter expression analyses in intact animals. Cell Tissue Res 327: 313-322.
53. Pellier V, Astic L. 1994. Histochemical and immunocytochemical study of the migration of neurons from the rat olfactory placode. Cell Tissue Res 275. 587-598.
54. Reiss JO, Burd GD. 1997. Cellular and molecular interactions in the development of the Xenopus olfactory system. Stem Cell Dev Biol 8: 171-179.
55. Sauka-Spengler T, Baratte B, Shi L, Mazan S. 2001. Structure and expression of an Otx5-related gene in the dogfish Scyliorhinus canicula: evidence for a conserved role of Otx5 and Crx genes in the specification of photoreceptors. Dev Genes Evol 211: 533-544.
56. Schluessel V, Bennett MB, Bleckmann H, Blomberg S, Collin SP. 2008. Morphometric and ultrastructural comparison of the olfactory system in elasmobranchs: the significance of structure-function relationships based on phylogeny and ecology. J Morphol 269: 1365-1386.
57. Schwanzel-Fukuda M, Pfaff DW. 1989. Origin of luteinizing hormone-releasing hormone neurons. Nature 338: 161-164.
58. Simpson TI, Price DJ. 2002. Pax6; a pleiotropic player in development. Bioessays 24: 1041-1051.
59. Stoykova A, Gruss P. 1994. Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J Neurosci 74: 1395-1412.
60. Takami S, Luer CA, Graziadei PPC. 1994. Microscopic structure of the olfactory organ of the clearnose skate, Raja eglanteria. Anat Embryol 190: 211-230.
61. Theisen B, Zeiske E, Breucker H. 1986. Functional morphology of the olfactory organs in the spiny dogfish (Squalus acanthias L.) and the small-spotted catshark (Scyliorhinus canicula L.). Acta Zool 67: 73-86.
62. Thieler K, Varnum DS, Stevens LC. 1978. Development of Dickie’s small eye, a mutation in the house mouse. Anat Embryol 155: 81-86.
63. Valverde F, Santacana M, Heredia M. 1992. Formation of an olfactory glomerulus: morphological aspects of development and organization. Neuroscience 49: 255-275.
64. Valverde F, Heredia M, Santacana M. 1993. Characterization of neuronal cell varieties migrating from the olfactory epithelium during prenatal development in the rat. Immunocytochemical study using antibodies against olfactory marker protein (OMP) and luteinizing hormone-releasing hormone (LH-RH). Dev Brain Res 71: 209-220.
65. Walther C, Gruss P. 1991. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113: 1435-1449.
66. Whitlock KE, Westerfield M. 1998. A transient population of neurons pioneers the olfactory pathway in the zebrafish. J Neurosci 18: 8919-8927.
67. Wray S, Grant P, Gainer H. 1989. Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode. Proc Natl Acad Sci USA 86: 8132-8136.
68. Wullimann MF, Rink E. 2001. Detailed immunohistology of Pax6 protein and tyrosine hydroxylase in the early zebrafish brain suggests role of Pax6 gene in development of dopaminergic diencephalic neurons. Dev Brain Res 131: 173-179.