Differentiation of apical and basal dendrites in pyramidal cells and granule cells in dissociated hippocampal cultures

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Wu, You Kure ^a   Fujishima, Kazuto ^b   Kengaku, Mineko ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL POLARITY; CELL SPECIFICITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; EMBRYO PATTERN FORMATION; GOLGI COMPLEX; GRANULE CELL; HIPPOCAMPAL NEURONAL CULTURE; INTERNEURON; INTRINSIC ACTIVITY; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOLECULAR STABILITY; MORPHOMETRICS; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NONHUMAN; PYRAMIDAL NERVE CELL; QUANTITATIVE STUDY; TIME LAPSE IMAGING; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CONFOCAL MICROSCOPY; CYTOLOGY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; NERVE CELL; PHYSIOLOGY; PRIMARY CELL CULTURE;

GLIAL FIBRILLARY ACIDIC PROTEIN; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; NERVE PROTEIN;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITES; DENTATE GYRUS; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE DECARBOXYLASE; GOLGI APPARATUS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICE, INBRED ICR; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NEURONS; PRIMARY CELL CULTURE; PYRAMIDAL CELLS; TIME-LAPSE IMAGING;

EID: 84923274861     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118482     Document Type: Article

References (51)

1. Seress L, Mrzljak L. Basal dendrites of granule cells are normal features of the fetal and adult dentate gyrus of both monkey and human hippocampal formations. Brain Res. 1987; 405:169-174. PMID: 3567591
2. Jones SP, Rahimi O, O'Boyle MP, Diaz DL, Claiborne BJ. Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3. Hippocampus. 2003; 13:413-427. PMID: 12722981
3. Shapiro LA, Ribak CE. Integration of newly born dentate granule cells into adult brains: hypotheses based on normal and epileptic rodents. Brain Res Brain Res Rev. 2005; 48:43-56. PMID: 15708627
4. McAllister AK, Lo DC, Katz LC. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron. 1995; 15:791-803. PMID: 7576629
5. Häusser M, Spruston N, Stuart GJ. Diversity and dynamics of dendritic signaling. Science. 2000; 290:739-744. PMID: 11052929
6. Arikkath J. Molecular mechanisms of dendrite morphogenesis. Front Cell Neurosci. 2012; 6:61. doi: 10.3389/fncel.2012.00061 PMID: 23293584
7. Polleux F, Morrow T, Ghosh A. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature. 2000; 404:567-573. PMID: 10766232
8. Fenstermaker V, Chen Y, Ghosh A, Yuste R. Regulation of dendritic length and branching by semaphorin 3A. J Neurobiol. 2004; 58:403-412. PMID: 14750152
9. Nakamura F, Ugajin K, Yamashita N, Okada T, Uchida Y, Taniguchi M, et al. Increased proximal bifurcation of CA1 pyramidal apical dendrites in sema3A mutant mice. J Comp Neurol. 2009; 516:360-375. doi: 10.1002/cne.22125 PMID: 19655386
10. Tran TS, Rubio ME, Clem RL, Johnson D, Case L, Tessier-Lavigne M, et al. Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. Nature. 2009; 462:1065-1069. doi: 10.1038/nature08628 PMID: 20010807
11. de Anda FC, Rosario AL, Durak O, Tran T, Gräff J, Meletis K, et al. Autism spectrum disorder susceptibility gene TAOK2 affects basal dendrite formation in the neocortex. Nat Neurosci. 2012; 15:1022-1031. doi: 10.1038/nn.3141 PMID: 22683681
12. Niisato E, Nagai J, Yamashita N, Nakamura F, Goshima Y, Ohshima T. Phosphorylation of CRMP2 is involved in proper bifurcation of the apical dendrite of hippocampal CA1 pyramidal neurons. Dev Neurobiol. 2012; 73:142-151. doi: 10.1002/dneu.22048 PMID: 22826151
13. Horton AC, Rácz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron. 2005; 48:757-771. PMID: 16337914
14. Matsuki T, Matthews RT, Cooper JA, van der Brug MP, Cookson MR, Hardy JA, et al. Reelin and stk25 have opposing roles in neuronal polarization and dendritic Golgi deployment. Cell. 2010; 143:826-836. doi: 10.1016/j.cell.2010.10.029 PMID: 21111240
15. Srivastava DP, Woolfrey KM, Jones KA, Anderson CT, Smith KR, Russell TA, et al. An autism-associated variant of Epac2 reveals a role for Ras/Epac2 signaling in controlling basal dendrite maintenance in mice. PLoS Biol. 2012; 10:e1001350. doi: 10.1371/journal.pbio.1001350 PMID: 22745599
16. Horton AC, Yi JJ, Ehlers MD. Cell type-specific dendritic polarity in the absence of spatially organized external cues. Brain Cell Biol. 2006; 35:29-38. PMID: 17940911
17. Baba A, Yamada MK, Nishiyama N, Matsuki N, Ikegaya Y. Different Ca2+ dynamics between isolated hippocampal pyramidal cells and dentate granule cells. J Neurocytol. 2002; 31:41-48. PMID: 12652086
18. nd ed. Cambridge: MIT press; 1998. PMID: 25506963
19. Kurisu J, Fukuda T, Yokoyama S, Hirano T, Kengaku M. Polarized targeting of DNER into dendritic plasma membrane in hippocampal neurons depends on endocytosis. J Neurochem. 2010; 113:1598-1610. doi: 10.1111/j.1471-4159.2010.06714.x PMID: 20367751
20. Eiraku M, Tohgo A, Ono K, Kaneko M, Fujishima K, Hirano T, et al. DNER acts as a neuron-specific Notch ligand during Bergmann glial development. Nat Neurosci. 2005; 8:873-880. PMID: 15965470
21. Fujishima K, Horie R, Mochizuki A, Kengaku M. Principles of branch dynamics governing shape characteristics of cerebellar Purkinje cell dendrites. Development. 2012; 139:3442-3455. doi: 10.1242/dev.081315 PMID: 22912417
22. Sampo B, Kaech S, Kunz S, Banker G. Two distinct mechanisms target membrane proteins to the axonal surface. Neuron. 2003; 37:611-624. PMID: 12597859
23. Das SS, Banker GA. The role of protein interaction motifs in regulating the polarity and clustering of the metabotropic glutamate receptor mGluR1a. J Neurosci. 2006; 26:8115-8125. PMID: 16885225
24. Bartholomä A, Nave KA. NEX-1: a novel brain-specific helix-loop-helix protein with autoregulation and sustained expression in mature cortical neurons. Mech Dev. 1994; 48:217-228. PMID: 7545978
25. Schwab MH, Bartholomae A, Heimrich B, Feldmeyer D, Druffel-Augustin S, Goebbels S, et al. 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. PMID: 10804213
26. 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. PMID: 17368742
27. Lavado A, Oliver G. Prox1 expression patterns in the developing and adult murine brain. Dev Dyn. 2007; 236:518-524. PMID: 17117441
28. Kaufman DL, Houser CR, Tobin AJ. Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J Neurochem. 1991; 56:720-723. PMID: 1988566
29. Bignami A, Eng LF, Dahl D, Uyeda CT. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 1972; 43:429-435. PMID: 4559710
30. Stanfield BB, Cowan WM The development of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol. 1979; 185:423-459. PMID: 86549
31. Altman J, Bayer SA. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol. 1990; 301:325-342. PMID: 2262594
32. Altman J, Bayer SA. 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. PMID: 2262595
33. Angevine JB. Time of neuron origin region in the hippocampal region: An autoradiographic study in the mouse. Exp Neurol Suppl. 1965; 2:1-70. PMID: 5838955
34. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, et al. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci. 2003; 24: 603-613. PMID: 14664811
35. Nakamura N, Rabouille C, Watson R, Nilsson T, Hui N, Slusarewicz P. et al. Characterization of a cis-Golgi matrix protein, GM130. J Cell Biol. 1995; 131:1715-1726. PMID: 8557739
36. Barr FA, Puype M, Vandekerckhove J, Warren G. GRASP65, a protein involved in the stacking of Golgi cisternae. Cell. 1997; 91:253-262. PMID: 9346242
37. Bayer SA. Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol. 1980; 190:87-114. PMID: 7381056
38. Galceran J, Miyashita-Lin EM, Devaney E, Rubenstein JL, Grosschedl R. Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development. 2000; 127:469-482. PMID: 10631168
39. Arnold SJ, Huang GJ, Cheung AFP, Era T, Nishikawa S, Bikoff EK, et al. The T-box transcription factor Eomes/Tbr2 regulates neurogenesis in the cortical subventricular zone. Genes Dev. 2008; 22:2479-2484. doi: 10.1101/gad.475408 PMID: 18794345
40. Galichet C, Guillemot F, Parras CM. Neurogenin 2 has an essential role in development of the dentate gyrus. Development. 2008; 135:2031-2041. doi: 10.1242/dev.015115 PMID: 18448566
41. Iwano T, Masuda A, Kiyonari H, Enomoto H, Matsuzaki F. Prox1 postmitotically defines dentate gyrus cells by specifying granule cell identity over CA3 pyramidal cell fate in the hippocampus. Development. 2012; 139:3051-3062. doi: 10.1242/dev.080002 PMID: 22791897
42. Spigelman I, Yan XX, Obenaus A, Lee EY, Wasterlain CG, Ribak CE. Dentate granule cells form novel basal dendrites in a rat model of temporal lobe epilepsy. Neuroscience. 1998; 86:109-120. PMID: 9692747
43. Ribak CE, Tran PH, Spigelman I, Okazaki MM, Nadler JV. Status epilepticus-induced hilar basal dendrites on rodent granule cells contribute to recurrent excitatory circuitry. J Comp Neurol. 2000; 428:240-253. PMID: 11064364
44. Patel LS, Wenzel HJ, Schwartzkroin PA. Physiological and morphological characterization of dentate granule cells in the p35 knock-out mouse hippocampus: evidence for an epileptic circuit. J Neurosci. 2004; 24:9005-9014. PMID: 15483119
45. Nakahara S, Tamura M, Matsuki N, Koyama R. Neuronal hyperactivity sustains the basal dendrites of immature dentate granule cells: time-lapse confocal analysis using hippocampal slice cultures. Hippocampus. 2009; 19:379-391. doi: 10.1002/hipo.20529 PMID: 19004014
46. Hatanaka Y, Murakami F. In vitro analysis of the origin, migratory behavior, and maturation of cortical pyramidal cells. J Comp Neurol. 2002; 454:1-14. PMID: 12410614
47. Nadarajah B, Alifragis P, Wong ROL, Parnavelas JG. Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb Cortex. 2003; 13:607-611. PMID: 12764035
48. 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. PMID: 15682392
49. Kitazawa A, Kubo K, Hayashi K, Matsunaga Y, Ishii K, Nakajima K. Hippocampal pyramidal neurons switch from a multipolar migration mode to a novel "climbing" migration mode during development. J Neurosci. 2014; 34:1115-1126. doi: 10.1523/JNEUROSCI.2254-13.2014 PMID: 24453304
50. Matsuki T, Pramatarova A, Howell BW. Reduction of Crk and CrkL expression blocks reelin-induced dendritogenesis. J Cell Sci. 2008; 121:1869-1875. doi: 10.1242/jcs.027334 PMID: 18477607
51. Meseke M, Rosenberger G, Förster E. Reelin and the Cdc42/Rac1 guanine nucleotide exchange factor αPIX/Arhgef6 promote dendritic Golgi translocation in hippocampal neurons. Eur J Neurosci. 2013; 37:1404-1412. doi: 10.1111/ejn.12153 PMID: 23406282