Different neural crest populations exhibit diverse proliferative behaviors

Developmental Neurobiology

Volumn 75, Issue 3, 2015, Pages 287-301

  Gonsalvez, David G ^a   Li Yuen Fong, Mathew ^a   Cane, Kylie N ^a   Stamp, Lincon A ^a   Young, Heather M ^a   Anderson, Colin R ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Dorsal root ganglia; Enteric nervous system; Neural crest; Peripheral nervous system; Proliferation

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL CYCLE G2 PHASE; CELL CYCLE PARAMETERS; CELL POPULATION; CELL PROLIFERATION; EMBRYO; EMBRYO DEVELOPMENT; FROZEN SECTION; GLIA CELL; INTESTINE INNERVATION; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL; SPINAL GANGLION; TISSUE SPECIFICITY; ANIMAL; C57BL MOUSE; CELL CYCLE; CYTOLOGY; EMBRYOLOGY; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

BIOLOGICAL MARKER; SOX10 PROTEIN, MOUSE; TRANSCRIPTION FACTOR SOX;

ANIMALS; BIOLOGICAL MARKERS; CELL CYCLE; CELL PROLIFERATION; ENTERIC NERVOUS SYSTEM; GANGLIA, SPINAL; MICE; MICE, INBRED C57BL; NEURAL CREST; NEUROGENESIS; SOXE TRANSCRIPTION FACTORS;

EID: 84922824299     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22229     Document Type: Article

References (82)

1. Arai Y, Pulvers JN, Haffner C, Schilling B, Nusslein I, Calegari F, Huttner WB. 2011. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun 2:154.
2. Armstrong A, Ryu YK, Chieco D, Kuruvilla R. 2011. Frizzled3 is required for neurogenesis and target innervation during sympathetic nervous system development. J Neurosci 31:2371-2381.
3. Baetge G, Gershon MD. 1989. Transient catecholaminergic cells in the vagus nerves and the bowel of fetal mice: Relationships to the development of enteric neurons. Dev Biol 132:189-211.
4. Baetge G, Pintar JE, Gershon MD. 1990. Transiently catecholaminergic (TC) cells in the bowel of the fetal rat: Precursors of noncatecholaminergic enteric neurons. Dev Biol 141:353-380.
5. Bergner AJ, Stamp LA, Gonsalvez DG, Allison MB, Olson DP, Myers MG, Anderson CR, et al. 2014. Birthdating of myenteric neuron subtypes in the small intestine of the mouse. J Comp Neurol 522:514-527.
6. Bravo R, Macdonald-Bravo H. 1987. Existence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle: Association with DNA replication sites. J Cell Biol 105:1549-1554.
7. Britsch S, Goerich DE, Riethmacher D, Peirano RI, Rossner M, Nave KA, Birchmeier C, et al. 2001. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 15:66-78.
8. Bronner ME, LeDouarin NM. 2012. Development and evolution of the neural crest: An overview. Developmental Biology 366:2-9.
9. Brown DC, Gatter KC. 2002. Ki67 protein: The immaculate deception? Histopathology 40:2-11.
10. Bruno S, Darzynkiewicz Z. 1992. Cell cycle dependent expression and stability of the nuclear protein detected by Ki-67 antibody in HL-60 cells. Cell Prolif 25:31-40.
11. Butler Tjaden NE, Trainor PA. 2013. The developmental etiology and pathogenesis of Hirschsprung disease. Transl Res 162:1-15.
12. Calegari F, Haubensak W, Haffner C, Huttner WB. 2005. Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J Neurosci 25:6533-6538.
13. Callahan T, Young HM, Anderson RB, Enomoto H, Anderson CR. 2008. Development of satellite glia in mouse sympathetic ganglia: GDNF and GFR alpha 1 are not essential. Glia 56:1428-1437.
14. Chubb DP, Anderson CR. 2010. The relationship of the birth date of rat sympathetic neurons to the target they innervate. Dev Dyn 239:897-904.
15. Conner PJ, Focke PJ, Noden DM, Epstein ML. 2003. Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells. Dev Dyn 226:91-98.
16. Dehay C, Kennedy H. 2007. Cell-cycle control and cortical development. Nat Rev Neurosci 8:438-450.
17. Dolatshad H, Cary AJ, Davis FC. 2010. Differential expression of the circadian clock in maternal and embryonic tissues of mice. PLoS One 5:e9855.
18. Eisch AJ, Mandyam CD. 2007. Adult neurogenesis: can analysis of cell cycle proteins move us "Beyond BrdU"? Curr Pharm Biotechnol 8:147-165.
19. Enomoto H, Crawford PA, Gorodinsky A, Heuckeroth RO, Johnson EM, Jr., Milbrandt J. 2001. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128:3963-3974.
20. Fairman CL, Clagett-Dame M, Lennon VA, Epstein ML. 1995. Appearance of neurons in the developing chick gut. Dev Dyn 204:192-201.
21. Fan YJ, Wu LL, Li HY, Wang YJ, Zhou XF. 2008. Differential effects of pro-BDNF on sensory neurons after sciatic nerve transection in neonatal rats. Eur J Neurosci 27:2380-2390.
22. Frank E, Sanes JR. 1991. Lineage of neurons and glia in chick dorsal root ganglia: Analysis in vivo with a recombinant retrovirus. Development 111:895-908.
23. Furness JB. 2012. The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 9:286-294.
24. Gianino S, Grider JR, Cresswell J, Enomoto H, Heuckeroth RO. 2003. GDNF availability determines enteric neuron number by controlling precursor proliferation. Development 130:2187-2198.
25. Gonsalvez DG, Cane KN, Landman KA, Enemoto H, Young HM, Anderson CR. 2013. Proliferation and cell cycle dynamics in the developing stellate ganglion. J Neurosci 33:5969-5979.
26. Hayes NL, Nowakowski RS. 2000. Exploiting the dynamics of S-phase tracers in developing brain: interkinetic nuclear migration for cells entering versus leaving the S-phase. Dev Neurosci 22:44-55.
27. Heidebrecht HJ, Buck F, Haas K, Wacker HH, Parwaresch R. 1996. Monoclonal antibodies Ki-S3 and Ki-S5 yield new data on the 'Ki-67' proteins. Cell Prolif 29:413-425.
28. Hjerling-Leffler J, Marmigere F, Heglind M, Cederberg A, Koltzenburg M, Enerback S, Ernfors P. 2005. The boundary cap: A source of neural crest stem cells that generate multiple sensory neuron subtypes. Development 132:2623-2632.
29. Inada Y, Uchida H, Umemura Y, Nakamura W, Sakai T, Koike N, Yagita K. 2014. Cell and tissue-autonomous development of the circadian clock in mouse embryos. FEBS Lett 588:459-465.
30. Kam MK, Cheung MC, Zhu JJ, Cheng WW, Sat EW, Tam PK, Lui VC. 2014. Perturbation of Hoxb5 signaling in vagal and trunk neural crest cells causes apoptosis and neurocristopathies in mice. Cell Death Differ 21:278-289.
31. Kurtz A, Zimmer A, Schnutgen F, Bruning G, Spener F, Muller T. 1994. The expression pattern of a novel gene encoding brain-fatty acid binding protein correlates with neuronal and glial cell development. Development 120:2637-2649.
32. Lange C, Calegari F. 2010. Cdks and cyclins link G1 length and differentiation of embryonic, neural and hematopoietic stem cells. Cell Cycle 9:1893-1900.
33. Lange C, Huttner WB, Calegari F. 2009. Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5:320-331.
34. Laranjeira C, Pachnis V. 2009. Enteric nervous system development: Recent progress and future challenges. Auton Neurosci 151:61-69.
35. Laranjeira C, Sandgren K, Kessaris N, Richardson W, Potocnik A, Vanden Berghe P, Pachnis V. 2011. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest 121:3412-3424.
36. Lawson SN, Biscoe TJ. 1979. Development of mouse dorsal root ganglia: An autoradiographic and quantitative study. J Neurocytol 8:265-274.
37. Lawson SN, Caddy KWT, Biscoe TJ. 1974. Development of rat dorsal root ganglion neurons-Studies of cell birthdays and changes in mean cell diameter. Cell Tissue Res 153:399-413.
38. Li Z, Caron MG, Blakely RD, Margolis KG, Gershon MD. 2010. Dependence of serotonergic and other nonadrenergic enteric neurons on norepinephrine transporter expression. J Neurosci 30:16730-16740.
39. Li Z, Chalazonitis A, Huang YY, Mann JJ, Margolis KG, Yang QM, Kim DO, et al. 2011. Essential roles of enteric neuronal serotonin in gastrointestinal motility and the development/survival of enteric dopaminergic neurons. J Neurosci 31:8998-9009.
40. Ma Q, Fode C, Guillemot F, Anderson DJ. 1999. Neurogenin1 and neurogenin2 control two distinct waves of neurogenesis in developing dorsal root ganglia. Genes Dev 13:1717-1728.
41. Mac Auley A, Werb Z, Mirkes PE. 1993. Characterization of the unusually rapid cell cycles during rat gastrulation. Development 117:873-883.
42. Mairet-Coello G, Tury A, Van Buskirk E, Robinson K, Genestine M, DiCicco-Bloom E. 2012. p57(KIP2) regulates radial glia and intermediate precursor cell cycle dynamics and lower layer neurogenesis in developing cerebral cortex. Development 139:475-487.
43. Marmigere F, Ernfors P. 2007. Specification and connectivity of neuronal subtypes in the sensory lineage. Nat Rev Neurosci 8:114-127.
44. Maro GS, Vermeren M, Voiculescu O, Melton L, Cohen J, Charnay P, Topilko P. 2004. Neural crest boundary cap cells constitute a source of neuronal and glial cells of the PNS. Nat Neurosci 7:930-938.
45. Martynoga B, Morrison H, Price DJ, Mason JO. 2005. Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev Biol 283:113-127.
46. McKeown SJ, Stamp L, Hao MM, Young HM. 2013. Hirschsprung disease: A developmental disorder of the enteric nervous system. Wiley Interdiscip Rev Dev Biol 2:113-129.
47. Memberg SP, Hall AK. 1995. Dividing neuron precursors express neuron-specific tubulin. J Neurobiol 27:26-43.
48. Miller MW, Nowakowski RS. 1988. Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res 457:44-52.
49. Mitsuhashi T, Takahashi T. 2009. Genetic regulation of proliferation/differentiation characteristics of neural progenitor cells in the developing neocortex. Brain Dev 31:553-557.
50. Montelius A, Marmigere F, Baudet C, Aquino JB, Enerback S, Ernfors P. 2007. Emergence of the sensory nervous system as defined by Foxs1 expression. Differentiation 75:404-417.
51. Nagashimada M, Ohta H, Li C, Nakao K, Uesaka T, Brunet JF, Amiel J, et al. 2012. Autonomic neurocristopathy-associated mutations in PHOX2B dysregulate Sox10 expression. J Clin Invest 122:3145-3158.
52. Nowakowski RS, Caviness VS, Jr., Takahashi T, Hayes NL. 2002. Population dynamics during cell proliferation and neuronogenesis in the developing murine neocortex. Results Probl Cell Differ 39:1-25.
53. Nowakowski RS, Lewin SB, Miller MW. 1989. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18:311-318.
54. Obermayr F, Hotta R, Enomoto H, Young HM. 2013. Development and developmental disorders of the enteric nervous system. Nat Rev Gastroenterol Hepatol 10:43-57.
55. Paratore C, Goerich DE, Suter U, Wegner M, Sommer L. 2001. Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128:3949-3961.
56. Pilaz LJ, Patti D, Marcy G, Ollier E, Pfister S, Douglas RJ, Betizeau M, et al. 2009. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc Natl Acad Sci USA 106:21924-21929.
57. Potten CS, Booth D, Cragg NJ, Tudor GL, O'Shea JA, Appleton D, Barthel D, et al. 2002. Cell kinetic studies in the murine ventral tongue epithelium: Thymidine metabolism studies and circadian rhythm determination. Cell Prolif 35(Suppl 1):1-15.
58. Ridenour DA, McLennan R, Teddy JM, Semerad CL, Haug JS, Kulesa PM. 2014. The neural crest cell cycle is related to phases of migration in the head. Development 141:1095-1103.
59. Rohrer H, Thoenen H. 1987. Relationship between differentiation and terminal mitosis: Chick sensory and ciliary neurons differentiate after terminal mitosis of precursor cells, whereas sympathetic neurons continue to divide after differentiation. J Neurosci 7:3739-3748.
60. Ross HH, Rahman M, Levkoff LH, Millette S, Martin-Carreras T, Dunbar EM, et al. 2011. Ethynyldeoxyuridine (EdU) suppresses in vitro population expansion and in vivo tumor progression of human glioblastoma cells. J Neurooncol 105:485-498.
61. Rothman TP, Gershon MD, Holtzer H. 1978. The relationship of cell division to the acquisition of adrenergic characteristics by developing sympathetic ganglion cell precursors. Dev Biol 65:322-341.
62. Rothman TP, Tennyson VM, Gershon MD. 1986. Colonization of the bowel by the precursors of enteric glia: Studies of normal and congenitally aganglionic mutant mice. J Comp Neurol 252:493-506.
63. Salomoni P, Calegari F. 2010. Cell cycle control of mammalian neural stem cells: Putting a speed limit on G1. Trends Cell Biol 20:233-243.
64. Savatier P, Huang S, Szekely L, Wiman KG, Samarut J. 1994. Contrasting patterns of retinoblastoma protein expression in mouse embryonic stem cells and embryonic fibroblasts. Oncogene 9:809-818.
65. Shi H, Cui H, Alam G, Gunning WT, Nestor A, Giovannucci D, Zhang M, et al. 2008. Nestin expression defines both glial and neuronal progenitors in postnatal sympathetic ganglia. J Comp Neurol 508:867-878.
66. Simpson MJ, Zhang DC, Mariani M, Landman KA, Newgreen DF. 2007. Cell proliferation drives neural crest cell invasion of the intestine. Dev Biol 302:553-568.
67. Singh AP, Schach U, Nusslein-Volhard C. 2014. Proliferation, dispersal and patterned aggregation of iridophores in the skin prefigure striped colouration of zebrafish. Nat Cell Biol 16:604-614.
68. Stead E, White J, Faast R, Conn S, Goldstone S, Rathjen J, Dhingra U, et al. 2002. Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities. Oncogene 21:8320-8333.
69. Takahashi T, Nowakowski RS, Caviness VS, Jr. 1992. BUdR as an S-phase marker for quantitative studies of cytokinetic behaviour in the murine cerebral ventricular zone. J Neurocytol 21:185-197.
70. Takahashi T, Nowakowski RS, Caviness VS, Jr. 1993. Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci 13:820-833.
71. Takahashi T, Nowakowski RS, Caviness VS, Jr. 1995. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15:6046-6057.
72. Tarui T, Takahashi T, Nowakowski RS, Hayes NL, Bhide PG, Caviness VS. 2005. Overexpression of p27 Kip 1, probability of cell cycle exit, and laminar destination of neocortical neurons. Cereb Cortex 15:1343-1355.
73. Taupin P. 2007. BrdU immunohistochemistry for studying adult neurogenesis: Paradigms, pitfalls, limitations, and validation. Brain Res Rev 53:198-214.
74. Tkatchenko AV, Walsh PA, Tkatchenko TV, Gustincich S, Raviola E. 2006. Form deprivation modulates retinal neurogenesis in primate experimental myopia. Proc Natl Acad Sci USA 103:4681-4686.
75. Trainor PA. 2010. Craniofacial birth defects: The role of neural crest cells in the etiology and pathogenesis of Treacher Collins syndrome and the potential for prevention. Am J Med Genet A 152A:2984-2994.
76. Wakamatsu Y, Maynard TM, Weston JA. 2000. Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis. Development 127:2811-2821.
77. Weigl Y, Ashkenazi IE, Peleg L. 2013. Rhythmic profiles of cell cycle and circadian clock gene transcripts in mice: A possible association between two periodic systems. J Exp Biol 216:2276-2282.
78. Woodhoo A, Dean CH, Droggiti A, Mirsky R, Jessen KR. 2004. The trunk neural crest and its early glial derivatives: A study of survival responses, developmental schedules and autocrine mechanisms. Mol Cell Neurosci 25:30-41.
79. Young HM, Bergner AJ, Muller T. 2003. Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J Comp Neurol 456:1-11.
80. Young HM, Ciampoli D, Hsuan J, Canty AJ. 1999. Expression of Ret-, p75(NTR)-, Phox2a-, Phox2b-, and tyrosine hydroxylase-immunoreactivity by undifferentiated neural crest-derived cells and different classes of enteric neurons in the embryonic mouse gut. Dev Dyn 216:137-152.
81. Young HM, Jones BR, McKeown SJ. 2002. The projections of early enteric neurons are influenced by the direction of neural crest cell migration. J Neurosci 22:6005-6018.
82. Young HM, Turner KN, Bergner AJ. 2005. The location and phenotype of proliferating neural-crest-derived cells in the developing mouse gut. Cell Tissue Res 320:1-9.