Neural progenitors organize in small-world networks to promote cell proliferation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 16, 2013, Pages

  Malmersjö, Seth ^a,b   Rebellato, Paola ^a   Smedler, Erik ^a   Planert, Henrike ^a   Kanatani, Shigeaki ^a,c   Liste, Isabel ^a   Nanou, Evanthia ^a   Sunner, Hampus ^a   Abdelhady, Shaimaa ^a   Zhang, Songbai ^a   Andäng, Michael ^a   El Manira, Abdeljabbar ^a   Silberberg, Gilad ^a   Arenas, Ernest ^a   Uhlén, Per ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CONNEXIN 43; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; CALCIUM SIGNALING; CELL PROLIFERATION; EMBRYONIC STEM CELL; GAP JUNCTION; MOUSE; NERVE CELL; NEURAL PROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

ANIMALS; BRAIN; CALCIUM; CALCIUM CHANNELS, L-TYPE; CELL PROLIFERATION; CONNEXIN 43; ELECTRICAL SYNAPSES; MICE; MICE, INBRED C57BL; MICROSCOPY, INTERFERENCE; MODELS, NEUROLOGICAL; NERVE NET; NEURAL STEM CELLS; PLASMIDS; RNA, SMALL INTERFERING;

EID: 84876217650     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220179110     Document Type: Article

References (57)

1. McCulloch W, Pitts W (1943) A logical calculus of the ideas immanent in nervous activity. Bull Math Biophys 5:115-133.
2. Dehaene S, Changeux JP (2011) Experimental and theoretical approaches to conscious processing. Neuron 70(2):200-227.
3. Albert R, Barabasi AL (2002) Statistical mechanics of complex networks. Rev Mod Phys 74(1):47-97.
4. Feldt S, Bonifazi P, Cossart R (2011) Dissecting functional connectivity of neuronal microcircuits: Experimental and theoretical insights. Trends Neurosci 34(5):225-236.
5. Barkai N, Leibler S (1997) Robustness in simple biochemical networks. Nature 387(6636):913-917.
6. Barabási AL, Oltvai ZN (2004) Network biology: Understanding the cell's functional organization. Nat Rev Genet 5(2):101-113.
7. Amaral LA, Scala A, Barthelemy M, Stanley HE (2000) Classes of small-world networks. Proc Natl Acad Sci USA 97(21):11149-11152.
8. Barabasi AL, Albert R (1999) Emergence of scaling in random networks. Science 286(5439):509-512.
9. Guimerà R, Mossa S, Turtschi A, Amaral LA (2005) The worldwide air transportation network: Anomalous centrality, community structure, and cities' global roles. Proc Natl Acad Sci USA 102(22):7794-7799.
10. Owens DF, Kriegstein AR (1998) Patterns of intracellular calcium fluctuation in precursor cells of the neocortical ventricular zone. J Neurosci 18(14):5374-5388.
11. Crépel V, et al. (2007) A parturition-associated nonsynaptic coherent activity pattern in the developing hippocampus. Neuron 54(1):105-120.
12. Peinado A, Yuste R, Katz LC (1993) Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 10(1):103-114.
13. Williams RW, Herrup K (1988) The control of neuron number. Annu Rev Neurosci 11: 423-453.
14. Arenas E (2010) Towards stem cell replacement therapies for Parkinson's disease. Biochem Biophys Res Commun 396(1):152-156.
15. Ban J, et al. (2007) Embryonic stem cell-derived neurons form functional networks in vitro. Stem Cells 25(3):738-749.
16. Ciccolini F, et al. (2003) Local and global spontaneous calcium events regulate neurite outgrowth and onset of GABAergic phenotype during neural precursor differentiation. J Neurosci 23(1):103-111.
17. Blankenship AG, Feller MB (2010) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11(1):18-29.
18. Spitzer NC (2006) Electrical activity in early neuronal development. Nature 444(7120): 707-712.
19. Wong RO, Chernjavsky A, Smith SJ, Shatz CJ (1995) Early functional neural networks in the developing retina. Nature 374(6524):716-718.
20. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: Dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4(7):517-529.
21. Webb SE, Miller AL (2006) Ca2+ signaling and early embryonic patterning during the blastula and gastrula periods of zebrafish and Xenopus development. Biochim Biophys Acta 1763(11):1192-1208.
22. Komuro H, Rakic P (1993) Modulation of neuronal migration by NMDA receptors. Science 260(5104):95-97.
23. Desfrere L, et al. (2009) Na, K-ATPase signal transduction triggers CREB activation and dendritic growth. Proc Natl Acad Sci USA 106(7):2212-2217.
24. Uhlén P, Fritz N (2010) Biochemistry of calcium oscillations. Biochem Biophys Res Commun 396(1):28-32.
25. Komuro H, Rakic P (1996) Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron 17(2):275-285.
26. Yacubova E, Komuro H (2002) Stage-specific control of neuronal migration by somatostatin. Nature 415(6867):77-81.
27. Söhl G, Maxeiner S, Willecke K (2005) Expression and functions of neuronal gap junctions. Nat Rev Neurosci 6(3):191-200.
28. Yeager M, Harris AL (2007) Gap junction channel structure in the early 21st century: facts and fantasies. Curr Opin Cell Biol 19(5):521-528.
29. Elias LA, Kriegstein AR (2008) Gap junctions: Multifaceted regulators of embryonic cortical development. Trends Neurosci 31(5):243-250.
30. Kunze A, et al. (2009) Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA 106(27):11336-11341.
31. Bruzzone R, Dermietzel R (2006) Structure and function of gap junctions in the developing brain. Cell Tissue Res 326(2):239-248.
32. Wiencken-Barger AE, Djukic B, Casper KB, McCarthy KD (2007) A role for Connexin43 during neurodevelopment. Glia 55(7):675-686.
33. Liu X, Hashimoto-Torii K, Torii M, Ding C, Rakic P (2010) Gap junctions/hemichannels modulate interkinetic nuclear migration in the forebrain precursors. J Neurosci 30(12): 4197-4209.
34. Liu X, Sun L, Torii M, Rakic P (2012) Connexin 43 controls the multipolar phase of neuronal migration to the cerebral cortex. Proc Natl Acad Sci USA 109(21):8280-8285.
35. Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR (2004) Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43(5):647-661.
36. Gu X, Olson EC, Spitzer NC (1994) Spontaneous neuronal calcium spikes and waves during early differentiation. J Neurosci 14(11 Pt 1):6325-6335.
37. Montoro RJ, Yuste R (2004) Gap junctions in developing neocortex: A review. Brain Res Brain Res Rev47(1-3):216-226.
38. Jäderstad J, et al. (2010) Communication via gap junctions underlies early functional and beneficial interactions between grafted neural stem cells and the host. Proc Natl Acad Sci USA 107(11):5184-5189.
39. Siegel F, Heimel JA, Peters J, Lohmann C (2012) Peripheral and central inputs shape network dynamics in the developing visual cortex in vivo. Curr Biol 22(3):253-258.
40. Yuste R, Nelson DA, Rubin WW, Katz LC (1995) Neuronal domains in developing neocortex: Mechanisms of coactivation. Neuron 14(1):7-17.
41. Bonifazi P, et al. (2009) GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 326(5958):1419-1424.
42. Fransson P, Aden U, Blennow M, Lagercrantz H (2011) The functional architecture of the infant brain as revealed by resting-state fMRI. Cereb Cortex 21(1):145-154.
43. Downes JH, et al. (2012) Emergence of a small-world functional network in cultured neurons. PLOS Comput Biol 8(5):e1002522.
44. Watts DJ, Strogatz SH (1998) Collective dynamics of 'small-world' networks. Nature 393(6684):440-442.
45. Borodinsky LN, et al. (2004) Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429(6991):523-530.
46. Garaschuk O, Linn J, Eilers J, Konnerth A (2000) Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci 3(5):452-459.
47. Ben-Ari Y (2001) Developing networks play a similar melody. Trends Neurosci 24(6): 353-360.
48. Juszczak GR, Swiergiel AH (2009) Properties of gap junction blockers and their behavioural, cognitive and electrophysiological effects: Animal and human studies. Prog Neuropsychopharmacol Biol Psychiatry 33(2):181-198.
49. Reaume AG, et al. (1995) Cardiac malformation in neonatal mice lacking connexin43. Science 267(5205):1831-1834.
50. Arumugam H, Liu X, Colombo PJ, Corriveau RA, Belousov AB (2005) NMDA receptors regulate developmental gap junction uncoupling via CREB signaling. Nat Neurosci 8(12):1720-1726.
51. Moore KA, Lemischka IR (2006) Stem cells and their niches. Science 311(5769):1880-1885.
52. Barberi T, et al. (2003) Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat Biotechnol 21 (10): 1200-1207.
53. Ying QL, Stavridis M, Griffiths D, Li M, Smith A (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21(2): 183-186.
54. Peterlin ZA, Kozloski J, Mao BQ, Tsiola A, Yuste R (2000) Optical probing of neuronal circuits with calcium indicators. Proc Natl Acad Sci USA 97(7):3619-3624.
55. Malmersjö S, et al. (2010) Ca2+ and cAMP signaling in human embryonic stem cell-derived dopamine neurons. Stem Cells Dev 19(9):1355-1364.
56. Uhlén P (2004) Spectral analysis of calcium oscillations. Sci STKE 2004(258):pl15.
57. Clauset A, Shalizi CR, Newman MEJ (2009) Power-law distributions in empirical data. SIAM Rev 51(4):661-703.