Development of circadian oscillators in neurosphere cultures during adult neurogenesis

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Malik, Astha ^a   Jamasbi, Roudabeh J ^a   Kondratov, Roman V ^b   Geusz, Michael E ^a  

^a BOWLING GREEN STATE UNIVERSITY   (United States)

^b CLEVELAND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PER1 PROTEIN; CULTURE MEDIUM; FORSKOLIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; GENE EXPRESSION; GLIA; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; MALE; MOUSE; MPER1 GENE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROSPHERE; NONHUMAN; SUBVENTRICULAR ZONE; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CULTURE MEDIUM; DRUG EFFECTS; PHYSIOLOGY; SUPRACHIASMATIC NUCLEUS; TRANSGENIC MOUSE;

MUS;

ANIMALS; CELL DIFFERENTIATION; CIRCADIAN RHYTHM; COLFORSIN; CULTURE MEDIA; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROGENESIS; SUPRACHIASMATIC NUCLEUS;

EID: 84926326956     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122937     Document Type: Article

References (70)

1. Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70: 687-702. doi: 10.1016/j.neuron.2011.05.001 PMID: 21609825
2. Duan X, Kang E, Liu CY, Ming GL, Song H (2008) Development of neural stem cell in the adult brain. Curr Opin Neurobiol 18: 108-115. doi: 10.1016/j.conb.2008.04.001 PMID: 18514504
3. Bouchard-Cannon P, Mendoza-Viveros L, Yuen A, Kaern M, Cheng HY (2013) The circadian molecular clock regulates adult hippocampal neurogenesis by controlling the timing of cell-cycle entry and exit. Cell Rep 5: 961-973. doi: 10.1016/j.celrep.2013.10.037 PMID: 24268780
4. Wang LM, Dragich JM, Kudo T, Odom IH, Welsh DK, et al. (2009) Expression of the circadian clock gene Period2 in the hippocampus: possible implications for synaptic plasticity and learned behaviour. ASN Neuro 1.
5. Granados-Fuentes D, Prolo LM, Abraham U, Herzog ED (2004) The suprachiasmatic nucleus entrains, but does not sustain, circadian rhythmicity in the olfactory bulb. J Neurosci 24: 615-619. PMID: 14736846
6. Konefal S, Elliot M, Crespi B (2013) The adaptive significance of adult neurogenesis: an integrative approach. Front Neuroanat 7: 21. doi: 10.3389/fnana.2013.00021 PMID: 23882188
7. Trounson A (2002) Human embryonic stem cells: mother of all cell and tissue types. Reprod Biomed Online 4 Suppl 1: 58-63. PMID: 12470337
8. Reick M, Garcia JA, Dudley C, McKnight SL (2001) NPAS2: an analog of clock operative in the mammalian forebrain. Science 293: 506-509. PMID: 11441147
9. Segall LA, Perrin JS, Walker CD, Stewart J, Amir S (2006) Glucocorticoid rhythms control the rhythm of expression of the clock protein, Period2, in oval nucleus of the bed nucleus of the stria terminalis and central nucleus of the amygdala in rats. Neuroscience 140: 753-757. PMID: 16678973
10. Conway-Campbell BL, Sarabdjitsingh RA, McKenna MA, Pooley JR, Kershaw YM, et al. (2010) Glucocorticoid ultradian rhythmicity directs cyclical gene pulsing of the clock gene period 1 in rat hippocampus. J Neuroendocrinol 22: 1093-1100. doi: 10.1111/j.1365-2826.2010.02051.x PMID: 20649850
11. Gilhooley MJ, Pinnock SB, Herbert J (2011) Rhythmic expression of per1 in the dentate gyrus is suppressed by corticosterone: implications for neurogenesis. Neurosci Lett 489: 177-181. doi: 10.1016/j.neulet.2010.12.011 PMID: 21163331
12. Abraham U, Prior JL, Granados-Fuentes D, Piwnica-Worms DR, Herzog ED (2005) Independent circadian oscillations of Period1 in specific brain areas in vivo and in vitro. J Neurosci 25: 8620-8626. PMID: 16177029
13. Granados-Fuentes D, Tseng A, Herzog ED (2006) A circadian clock in the olfactory bulb controls olfactory responsivity. J Neurosci 26: 12219-12225. PMID: 17122046
14. Hamada T, Honma S, Honma K (2011) Light responsiveness of clock genes, Per1 and Per2, in the olfactory bulb of mice. Biochem Biophys Res Commun 409: 727-731. doi: 10.1016/j.bbrc.2011.05.076 PMID: 21624349
15. Granados-Fuentes D, Saxena MT, Prolo LM, Aton SJ, Herzog ED (2004) Olfactory bulb neurons express functional, entrainable circadian rhythms. Eur J Neurosci 19: 898-906. PMID: 15009137
16. Sun W, Kim H, Moon Y (2010) Control of neuronal migration through rostral migration stream in mice. Anat Cell Biol 43: 269-279. doi: 10.5115/acb.2010.43.4.269 PMID: 21267400
17. Yokoyama TK, Mochimaru D, Murata K, Manabe H, Kobayakawa K, et al. (2011) Elimination of adultborn neurons in the olfactory bulb is promoted during the postprandial period. Neuron 71: 883-897. doi: 10.1016/j.neuron.2011.05.046 PMID: 21903081
18. Belnoue L, Grosjean N, Abrous DN, Koehl M (2011) A critical time window for the recruitment of bulbar newborn neurons by olfactory discrimination learning. J Neurosci 31: 1010-1016. doi: 10.1523/JNEUROSCI.3941-10.2011 PMID: 21248125
19. Nolasco N, Juarez C, Morgado E, Meza E, Caba M (2012) A circadian clock in the olfactory bulb anticipates feeding during food anticipatory activity. PLoS One 7: e47779. doi: 10.1371/journal.pone. 0047779 PMID: 23094084
20. Yagita K, Horie K, Koinuma S, Nakamura W, Yamanaka I, et al. (2010) Development of the circadian oscillator during differentiation of mouse embryonic stem cells in vitro. Proc Natl Acad Sci U S A 107: 3846-3851. doi: 10.1073/pnas.0913256107 PMID: 20133594
21. Morse D, Cermakian N, Brancorsini S, Parvinen M, Sassone-Corsi P (2003) No circadian rhythms in testis: Period1 expression is clock independent and developmentally regulated in the mouse. Mol Endocrinol 17: 141-151. PMID: 12511614
22. Gimble JM, Floyd ZE, Bunnell BA (2009) The 4th dimension and adult stem cells: Can timing be everything? J Cell Biochem 107: 569-578. doi: 10.1002/jcb.22153 PMID: 19384905
23. Jain S, Maltepe E, Lu MM, Simon C, Bradfield CA (1998) Expression of ARNT, ARNT2, HIF1 alpha, HIF2 alpha and Ah receptor mRNAs in the developing mouse. Mech Dev 73: 117-123. PMID: 9545558
24. D'Ippolito G, Diabira S, Howard GA, Roos BA, Schiller PC (2006) Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 39: 513-522. PMID: 16616713
25. Doi M, Hirayama J, Sassone-Corsi P (2006) Circadian regulator CLOCK is a histone acetyltransferase. Cell 125: 497-508. PMID: 16678094
26. Asher G, Gatfield D, Stratmann M, Reinke H, Dibner C, et al. (2008) SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134: 317-328. doi: 10.1016/j.cell.2008.06.050 PMID: 18662546
27. Grechez-Cassiau A, Rayet B, Guillaumond F, Teboul M, Delaunay F (2008) The circadian clock component BMAL1 is a critical regulator of p21WAF1/CIP1 expression and hepatocyte proliferation. J Biol Chem 283: 4535-4542. PMID: 18086663
28. Baksh D, Boland GM, Tuan RS (2007) Cross-talk between Wnt signaling pathways in human mesenchymal stem cells leads to functional antagonism during osteogenic differentiation. J Cell Biochem 101: 1109-1124. PMID: 17546602
29. Baksh D, Tuan RS (2007) Canonical and non-canonical Wnts differentially affect the development potential of primary isolate of human bone marrow mesenchymal stem cells. J Cell Physiol 212: 817-826. PMID: 17458904
30. Iitaka C, Miyazaki K, Akaike T, Ishida N (2005) A role for glycogen synthase kinase-3beta in the mammalian circadian clock. J Biol Chem 280: 29397-29402. PMID: 15972822
31. Marshall GP 2nd, Reynolds BA, Laywell ED (2007) Using the neurosphere assay to quantify neural stem cells in vivo. Curr Pharm Biotechnol 8: 141-145. PMID: 17584087
32. Rietze RL, Reynolds BA (2006) Neural stem cell isolation and characterization. Methods Enzymol 419: 3-23. PMID: 17141049
33. Lundkvist GB, Kwak Y, Davis EK, Tei H, Block GD (2005) A calcium flux is required for circadian rhythm generation in mammalian pacemaker neurons. J Neurosci 25: 7682-7686. PMID: 16107654
34. Ahn JM, Lee CH, Kim DY, Rhee CS, Min YG, et al. (2008) Maintenance of regional difference in cellular composition of neurospheres derived from adult mouse olfactory bulb. Eur Arch Otorhinolaryngol 265: 429-434. PMID: 17938947
35. Silvestroff L, Franco PG, Pasquini JM (2012) ApoTransferrin: dual role on adult subventricular zone-derived neurospheres. PLoS ONE 7: e33937. doi: 10.1371/journal.pone.0033937 PMID: 22479482
36. Sousa-Ferreira L, Alvaro AR, Aveleira C, Santana M, Brandao I, et al. (2011) Proliferative hypothalamic neurospheres express NPY, AGRP, POMC, CART and Orexin-A and differentiate to functional neurons. PLoS ONE 6: e19745. doi: 10.1371/journal.pone.0019745 PMID: 21589937
37. Theocharatos S, Wilkinson DJ, Darling S, Wilm B, Kenny SE, et al. (2013) Regulation of progenitor cell proliferation and neuronal differentiation in enteric nervous system neurospheres. PLoS ONE 8: e54809. doi: 10.1371/journal.pone.0054809 PMID: 23372773
38. Hiler DJ, Bhattacherjee A, Yamazaki S, Tei H, Geusz ME (2008) Circadian mPer1 gene expression in mesencephalic trigeminal nucleus cultures. Brain Res 1214: 84-93. doi: 10.1016/j.brainres.2008.03.041 PMID: 18472091
39. Sharma VP, Anderson NT, Geusz ME (2014) Circadian properties of cancer stem cells in glioma cell cultures and tumorspheres. Cancer Lett 345: 65-74. doi: 10.1016/j.canlet.2013.11.009 PMID: 24333739
40. Abe M, Herzog ED, Yamazaki S, Straume M, Tei H, et al. (2002) Circadian rhythms in isolated brain regions. J Neurosci 22: 350-356. PMID: 11756518
41. Torrado EF, Gomes C, Santos G, Fernandes A, Brites D, et al. (2014) Directing mouse embryonic neurosphere differentiation toward an enriched neuronal population. Int J Dev Neurosci 37: 94-99. doi: 10.1016/j.ijdevneu.2014.07.001 PMID: 25016067
42. Tran PB, Banisadr G, Ren D, Chenn A, Miller RJ (2007) Chemokine receptor expression by neural progenitor cells in neurogenic regions of mouse brain. J Comp Neurol 500: 1007-1033. PMID: 17183554
43. Walker TL, Yasuda T, Adams DJ, Bartlett PF (2007) The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci 27: 3734-3742. PMID: 17409237
44. Burgess A, Wainwright SR, Shihabuddin LS, Rutishauser U, Seki T, et al. (2008) Polysialic acid regulates the clustering, migration, and neuronal differentiation of progenitor cells in the adult hippocampus. Dev Neurobiol 68: 1580-1590. doi: 10.1002/dneu.20681 PMID: 18844212
45. Kawakita E, Hashimoto M, Shido O (2006) Docosahexaenoic acid promotes neurogenesis in vitro and in vivo. Neuroscience 139: 991-997. PMID: 16527422
46. Takahashi J, Palmer TD, Gage FH (1999) Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J Neurobiol 38: 65-81. PMID: 10027563
47. Yagita K, Okamura H (2000) Forskolin induces circadian gene expression of rPer1, rPer2 and dbp in mammalian rat-1 fibroblasts. Febs Letters 465: 79-82. PMID: 10620710
48. Kimiwada T, Sakurai M, Ohashi H, Aoki S, Tominaga T, et al. (2009) Clock genes regulate neurogenic transcription factors, including NeuroD1, and the neuronal differentiation of adult neural stem/progenitor cells. Neurochemistry International 54: 277-285. doi: 10.1016/j.neuint.2008.12.005 PMID: 19121353
49. Guilding C, Piggins HD (2007) Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain? Eur J Neurosci 25: 3195-3216. PMID: 17552989
50. Beaule C, Swanstrom A, Leone MJ, Herzog ED (2009) Circadian modulation of gene expression, but not glutamate uptake, in mouse and rat cortical astrocytes. PLoS ONE 4: e7476. doi: 10.1371/journal. pone.0007476 PMID: 19829696
51. Imbeault S, Gauvin LG, Toeg HD, Pettit A, Sorbara CD, et al. (2009) The extracellular matrix controls gap junction protein expression and function in postnatal hippocampal neural progenitor cells. BMC Neurosci 10: 13. doi: 10.1186/1471-2202-10-13 PMID: 19236721
52. Vik-Mo EO, Sandberg C, Joel M, Stangeland B, Watanabe Y, et al. (2011) A comparative study of the structural organization of spheres derived from the adult human subventricular zone and glioblastoma biopsies. Exp Cell Res 317: 1049-1059. doi: 10.1016/j.yexcr.2010.12.022 PMID: 21199649
53. Wreschnig D, Dolatshad H, Davis FC (2014) Embryonic development of circadian oscillations in the mouse hypothalamus. J Biol Rhythms 29: 299-310. doi: 10.1177/0748730414545086 PMID: 25238858
54. Prolo LM, Takahashi JS, Herzog ED (2005) Circadian rhythm generation and entrainment in astrocytes. J Neurosci 25: 404-408. PMID: 15647483
55. Ng FS, Tangredi MM, Jackson FR (2011) Glial cells physiologically modulate clock neurons and circadian behavior in a calcium-dependent manner. Curr Biol 21: 625-634. doi: 10.1016/j.cub.2011.03.027 PMID: 21497088
56. Duhart JM, Leone MJ, Paladino N, Evans JA, Castanon-Cervantes O, et al. (2013) Suprachiasmatic astrocytes modulate the circadian clock in response to TNF-alpha. J Immunol 191: 4656-4664. doi: 10.4049/jimmunol.1300450 PMID: 24062487
57. Kowalska E, Moriggi E, Bauer C, Dibner C, Brown SA (2010) The circadian clock starts ticking at a developmentally early stage. J Biol Rhythms 25: 442-449. doi: 10.1177/0748730410385281 PMID: 21135160
58. Alvarez JD, Chen D, Storer E, Sehgal A (2003) Non-cyclic and developmental stage-specific expression of circadian clock proteins during murine spermatogenesis. Biol Reprod 69: 81-91. PMID: 12606319
59. Whitman MC, Greer CA (2009) Adult neurogenesis and the olfactory system. Prog Neurobiol 89: 162-175. doi: 10.1016/j.pneurobio.2009.07.003 PMID: 19615423
60. Lim DA, Alvarez-Buylla A (2014) Adult neural stem cells stake their ground. Trends Neurosci 37: 563-571. doi: 10.1016/j.tins.2014.08.006 PMID: 25223700
61. Granados-Fuentes D, Ben-Josef G, Perry G, Wilson DA, Sullivan-Wilson A, et al. (2011) Daily rhythms in olfactory discrimination depend on clock genes but not the suprachiasmatic nucleus. J Biol Rhythms 26: 552-560. doi: 10.1177/0748730411420247 PMID: 22215613
62. Moriya T, Hiraishi K, Horie N, Mitome M, Shinohara K (2007) Correlative association between circadian expression of mousePer2 gene and the proliferation of the neural stem cells. Neuroscience 146: 494-498. PMID: 17368741
63. Borgs L, Beukelaers P, Vandenbosch R, Nguyen L, Moonen G, et al. (2009) Period 2 regulates neural stem/progenitor cell proliferation in the adult hippocampus. BMC Neurosci 10: 30. doi: 10.1186/1471-2202-10-30 PMID: 19327139
64. Kageyama R, Yoshiura S, Masamizu Y, Niwa Y (2007) Ultradian oscillators in somite segmentation and other biological events. Cold Spring Harb Symp Quant Biol 72: 451-457. doi: 10.1101/sqb.2007.72.012 PMID: 18419304
65. Ueshima T, Kawamoto T, Honda KK, Noshiro M, Fujimoto K, et al. (2012) Identification of a new clockrelated element EL-box involved in circadian regulation by BMAL1/CLOCK and HES1. Gene 510: 118-125. doi: 10.1016/j.gene.2012.08.022 PMID: 22960268
66. Morgan R (2004) Pax6 is a direct, positively regulated target of the circadian gene Clock. Dev Dyn 230: 643-650. PMID: 15254898
67. Gan Q, Lee A, Suzuki R, Yamagami T, Stokes A, et al. (2014) Pax6 mediates beta-catenin signaling for self-renewal and neurogenesis by neocortical radial glial stem cells. Stem Cells 32: 45-58. doi: 10.1002/stem.1561 PMID: 24115331
68. Sansom SN, Griffiths DS, Faedo A, Kleinjan DJ, Ruan Y, et al. (2009) The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet 5: e1000511. doi: 10.1371/journal.pgen.1000511 PMID: 19521500
69. Curto GG, Nieto-Estevez V, Hurtado-Chong A, Valero J, Gomez C, et al. (2014) Pax6 is essential for the maintenance and multi-lineage differentiation of neural stem cells, and for neuronal incorporation into the adult olfactory bulb. Stem Cells Dev 23: 2813-2830. doi: 10.1089/scd.2014.0058 PMID: 25117830
70. Kondratova AA, Kondratov RV (2012) The circadian clock and pathology of the ageing brain. Nat Rev Neurosci 13: 325-335. doi: 10.1038/nrn3208 PMID: 22395806