Defining structural homology between the mammalian and avian hippocampus through conserved gene expression patterns observed in the chick embryo

Developmental Biology

Volumn 366, Issue 2, 2012, Pages 125-141

  Gupta, Sandeep ^a   Maurya, Reshma ^a   Saxena, Monika ^a   Sen, Jonaki ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY KANPUR   (India)

Author keywords

Chicken; Development; Hippocampus; Migration; Neurogenesis

Indexed keywords

HOMEODOMAIN PROTEIN; LYMPHOID ENHANCER FACTOR 1; NEUROPILIN 2; PROSPERO HOMEOBOX PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; CELL COUNT; CELL CYCLE S PHASE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO PATTERN FORMATION; ETV1 GENE; FOREBRAIN; GENE; GENE EXPRESSION; GENE FUNCTION; HIPPOCAMPUS; HUMAN; INTERNEURON; LEF1 GENE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROD GENE; NONHUMAN; PRIMORDIUM; PRIORITY JOURNAL; PROX1 GENE; STRUCTURAL HOMOLOGY;

AVES; MAMMALIA; MUS;

EID: 84861221325     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.03.027     Document Type: Article

References (73)

1. Altman J., Bayer S.A. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J. Comp. Neurol. 1990, 301:365-381.
2. Altman J., Bayer S.A. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J. Comp. Neurol. 1990, 301:325-342.
3. Altman J., Bayer S.A. Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale. J. Comp. Neurol. 1990, 301:343-364.
4. Altman J., Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 1965, 124:319-335.
5. Altman J., Das G.D. Post-natal origin of microneurones in the rat brain. Nature 1965, 207:953-956.
6. Altman J., Das G.D. Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J. Comp. Neurol. 1966, 126:337-389.
7. Atoji Y., Wild J.M. Anatomy of the avian hippocampal formation. Rev. Neurosci. 2006, 17:3-15.
8. Atoji Y, Wild J.M. Fiber connections of the hippocampal formation and septum and subdivisions of the hippocampal formation in the pigeon as revealed by tract tracing and kainic acid lesions. J. Comp. Neurol. 2004, 475:426-461.
9. Bagri A., Gurney T., He X., Zou Y.R., Littman D.R., Tessier-Lavigne M., Pleasure S.J. The chemokine SDF1 regulates migration of dentate granule cells. Development 2002, 129:4249-4260.
10. Bayer S.A. Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J. Comp. Neurol. 1980, 190:87-114.
11. Bayer S.A., Altman J. Hippocampal development in the rat: cytogenesis and morphogenesis examined with autoradiography and low-level X-irradiation. J. Comp. Neurol. 1974, 158:55-79.
12. Bingman V. Hippocampal lesions impair navigational learning in experienced homing pigeons. Behav. Neurosci. 1992, 106:229-232.
13. Bingman V.P., Gagliardo A., Hough G.E., Ioalé P., Kahn M.C., Siegel J.J. The avian hippocampus, homing in pigeons and the memory representation of large-scale space. Integr. Comp. Biol. 2005, 45:555-564.
14. Budzynski CA, G.A., Ioale P., Bingman VP. Participation of the homing pigeon thalamofugal visual pathway in sun-compass associative learning. Eur. J. Neurosci. 2002, 197-210.
15. Buss R.R., Sun W., Oppenheim R.W. Adaptive roles of programmed cell death during nervous system development. Annu. Rev. Neurosci. 2006, 29:1-35.
16. Cameron H.A., McKay R. Stem cells and neurogenesis in the adult brain. Curr. Opin. Neurobiol. 1998, 8:677-680.
17. Charvet C.J., Striedter G.F. Spatiotemporal clustering of cell death in the avian forebrain proliferative zone. Int. J. Dev. Biol. 2008, 52:345-352.
18. Chen H., Chedotal A., He Z., Goodman C.S., Tessier-Lavigne M. Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 1997, 19:547-559.
19. Clarke P.G., Posada A., Primi M.P., Castagne V. Neuronal death in the central nervous system during development. Biomed. Pharmacother. 1998, 52:356-362.
20. Cobos I., Puelles L., Martinez S. The avian telencephalic subpallium originates inhibitory neurons that invade tangentially the pallium (dorsal ventricular ridge and cortical areas). Dev. Biol. 2001, 239:30-45.
21. Colombo M., Broadbent N. Is the avian hippocampus a functional homologue of the mammalian hippocampus?. Neurosci. Biobehav. Rev. 2000, 24:465-484.
22. Craigie E.H. The cerebral hemispheres of the Kiwi and of the Emu (Apteryx and Dromiceius). J. Anat. 1935, 69:380-393.
23. Erichsen J.T., Bingman V.P., Krebs J.R. The distribution of neuropeptides in the dorsomedial telencephalon of the pigeon (Columba livia): a basis for regional subdivisions. J. Comp. Neurol. 1991, 314:478-492.
24. Galceran J., Miyashita-Lin E.M., Devaney E., Rubenstein J.L., Grosschedl R. Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development 2000, 127:469-482.
25. Galeeva A., Treuter E., Tomarev S., Pelto-Huikko M. A prospero-related homeobox gene Prox-1 is expressed during postnatal brain development as well as in the adult rodent brain. Neuroscience 2007, 146:604-616.
26. Gohlke J.M., Griffith W.C., Faustman E.M. The role of cell death during neocortical neurogenesis and synaptogenesis: implications from a computational model for the rat and mouse. Dev. Brain Res. 2004, 151:43-54.
27. Grove E.A., Tole S. Patterning events and specification signals in the developing hippocampus. Cereb. Cortex 1999, 9:551-561.
28. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. 1951. Dev. Dyn. 1992, 195:231-272.
29. Holash J.A., Pasquale E.B. Polarized expression of the receptor protein tyrosine kinase Cek5 in the developing avian visual system. Dev. Biol. 1995, 172:683-693.
30. Källen B. Embryogenesis of brain nuclei in the chick telencephalon. Ergeb. Anat. Entwicklungsgesch. 1962, 36:62-82.
31. Kahn M.C., Hough G.E., Ten Eyck G.R., Bingman V.P. Internal connectivity of the homing pigeon (Columba livia) hippocampal formation: an anterograde and retrograde tracer study. J. Comp. Neurol. 2003, 459:127-141.
32. Karten H.J., Hodos W. A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia) 1967, Johns Hopkins University Press, Baltimore, MD.
33. Kempermann G., Kuhn H.G., Gage F.H. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc. Natl. Acad. Sci. USA 1997, 94:10409-10414.
34. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
35. Kengaku M., Capdevila J., Rodriguez-Esteban C., De La Pena J., Johnson R.L., Izpisua Belmonte J.C., Tabin C.J. Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 1998, 280:1274-1277.
36. Kohler T., Prols F., Brand-Saberi B. PCNA in situ hybridization: a novel and reliable tool for detection of dynamic changes in proliferative activity. Histochem. Cell Biol. 2005, 123:315-327.
37. Krebs J.R., Erichsen J.T., Bingman V.P. The distribution of neurotransmitters and neurotransmitter-related enzymes in the dorsomedial telencephalon of the pigeon (Columba livia). J. Comp. Neurol. 1991, 314:467-477.
38. Kuhlenbeck H. The ontogenetic development and phylogenetic significance of the cortex telencephali in the chick. J. Comp. Neurol. 1938, 69:273-301.
39. Lavado A., Lagutin O.V., Chow L.M., Baker S.J., Oliver G. Prox1 is required for granule cell maturation and intermediate progenitor maintenance during brain neurogenesis. PLoS Biol. 2010, 8.
40. Lavado A., Oliver G. Prox1 expression patterns in the developing and adult murine brain. Dev. Dyn. 2007, 236:518-524.
41. Lee J.E., Hollenberg S.M., Snider L., Turner D.L., Lipnick N., Weintraub H. Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 1995, 268:836-844.
42. Lein E.S., Zhao X., Gage F.H. Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J. Neurosci. 2004, 24:3879-3889.
43. Liebl D.J., Morris C.J., Henkemeyer M., Parada L.F. mRNA Expression of ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system. J. Neurosci. Res. 2003, 71:7-22.
44. Lorente de No R. Studies on the structure of the cerebral cortex II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 1934, 46:113-177.
45. Margrie T.W., Rostas J.A., Sah P. Long-term potentiation of synaptic transmission in the avian hippocampus. J. Neurosci. 1998, 18:1207-1216.
46. Matsuda T., Cepko C.L. Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc. Natl. Acad. Sci. USA 2004, 101:16-22.
47. Miyata T., Maeda T., Lee J.E. NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev. 1999, 13:1647-1652.
48. Molla R., Rodriguez J., Calvet S., Garcia-Verdugo J.M. Neuronal types of the cerebral cortex of the adult chicken (Gallus gallus). A Golgi study. J. Hirnforsch. 1986, 27:381-390.
49. Montagnese C.M., Krebs J.R., Meyer G. The dorsomedial and dorsolateral forebrain of the zebra finch, Taeniopygia guttata: a Golgi study. Cell Tissue Res. 1996, 283:263-282.
50. Nakahira E., Yuasa S. Neuronal generation, migration, and differentiation in the mouse hippocampal primoridium as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation. J. Comp. Neurol. 2005, 483:329-340.
51. Nikolakopoulou A.M., Parpas A., Panagis L., Zikopoulos B., Dermon C.R. Early post-hatching sex differences in cell proliferation and survival in the quail telencephalic ventricular zone and intermediate medial mesopallium. Brain Res. Bull. 2006, 70:107-116.
52. Oliver G., Sosa-Pineda B., Geisendorf S., Spana E.P., Doe C.Q., Gruss P. Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech. Dev. 1993, 44:3-16.
53. Pleasure S.J., Collins A.E., Lowenstein D.H. Unique expression patterns of cell fate molecules delineate sequential stages of dentate gyrus development. J. Neurosci. 2000, 20:6095-6105.
54. Redies C., Medina L., Puelles L. Cadherin expression by embryonic divisions and derived gray matter structures in the telencephalon of the chicken. J. Comp. Neurol. 2001, 438:253-285.
55. Rodriguez F., Lopez J.C., Vargas J.P., Gomez Y., Broglio C., Salas C. Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. J. Neurosci. 2002, 22:2894-2903.
56. Sandi C., Rose S.P., Patterson T.A. Unilateral hippocampal lesions prevent recall of a passive avoidance task in day-old chicks. Neurosci. Lett. 1992, 141:255-258.
57. Schwab M.H., Bartholomae A., Heimrich B., Feldmeyer D., Druffel-Augustin S., Goebbels S., Naya F.J., Zhao S., Frotscher M., Tsai M.J., Nave K.A. Neuronal basic helix-loop-helix proteins (NEX and BETA2/Neuro D) regulate terminal granule cell differentiation in the hippocampus. J. Neurosci. 2000, 20:3714-3724.
58. Sherry D.F., Vaccarino A.L Hippocampus and memory for food caches in black-capped chickadees. Behav. Neurosci. 1989, 308-318.
59. Siegel J.J., Nitz D., Bingman V.P. Hippocampal theta rhythm in awake, freely moving homing pigeons. Hippocampus 2000, 10:627-631.
60. Siegel J.J., Nitz D., Bingman V.P. Electrophysiological profile of avian hippocampal unit activity: a basis for regional subdivisions. J. Comp. Neurol. 2002, 445:256-268.
61. Smith C.A., Roeszler K.N., Ohnesorg T., Cummins D.M., Farlie P.G., Doran T.J., Sinclair A.H. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 2009, 461:267-271.
62. Striedter G.F., Keefer B.P. Cell migration and aggregation in the developing telencephalon: pulse-labeling chick embryos with bromodeoxyuridine. J. Neurosci. 2000, 20:8021-8030.
63. Suge R., McCabe B.J. Early stages of memory formation in filial imprinting: Fos-like immunoreactivity and behavior in the domestic chick. Neuroscience 2004, 123:847-856.
64. Szekely AD, K.J Efferent connectivity of the hippocampal formation of the zebra finch (Taeniopygia guttata): an anterograde pathway tracing study using Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 1996, 198-214.
65. Szele F.G., Cepko C.L. A subset of clones in the chick telencephalon arranged in rostrocaudal arrays. Curr. Biol. 1996, 6:1685-1690.
66. Thomaidou D., Mione M.C., Cavanagh J.F., Parnavelas J.G. Apoptosis and its relation to the cell cycle in the developing cerebral cortex. J. Neurosci. 1997, 17:1075-1085.
67. Tole S., Christian C., Grove E.A. Early specification and autonomous development of cortical fields in the mouse hippocampus. Development 1997, 124:4959-4970.
68. Tombol T., Davies D.C., Nemeth A., Sebesteny T., Alpar A. A comparative Golgi study of chicken (Gallus domesticus) and homing pigeon (Columba livia) hippocampus. Anat. Embryol. (Berlin) 2000, 201:85-101.
69. Trimarchi J.M., Stadler M.B., Roska B., Billings N., Sun B., Bartch B., Cepko C.L. Molecular heterogeneity of developing retinal ganglion and amacrine cells revealed through single cell gene expression profiling. J. Comp. Neurol. 2007, 502:1047-1065.
70. Tsai H.M., Garber B.B., Larramendi L.M. 3H-thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo: I. Neuronal birthdates of telencephalic compartments in situ. J. Comp. Neurol. 1981, 198:275-292.
71. Wilkie A.L., Jordan S.A., Sharpe J.A., Price D.J., Jackson I.J. Widespread tangential dispersion and extensive cell death during early neurogenesis in the mouse neocortex. Dev. Biol. 2004, 267:109-118.
72. Yoneshima H., Yamasaki S., Voelker C.C., Molnar Z., Christophe E., Audinat E., Takemoto M., Nishiwaki M., Tsuji S., Fujita I., Yamamoto N. Er81 is expressed in a subpopulation of layer 5 neurons in rodent and primate neocortices. Neuroscience 2006, 137:401-412.
73. Zhang S., Su Y., Shinmyo Y., Islam S.M., Naser I.B., Ahmed G., Tamamaki N., Tanaka H. Draxin, a repulsive axon guidance protein, is involved in hippocampal development. Neurosci. Res. 2010, 66:53-61.