Dendrite complexity of sympathetic neurons is controlled during postnatal development by BMP signaling

Journal of Neuroscience

Volumn 33, Issue 38, 2013, Pages 15132-15144

  Majdazari, Afsaneh ^a   Stubbusch, Jutta ^a   Müller, Christian M ^b   Hennchen, Melanie ^a   Weber, Marlen ^a   Deng, Chu Xia ^c   Mishina, Yuji ^d   Schütz, Günther ^e   Deller, Thomas ^b   Rohrer, Hermann ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; ACTIVIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN; GROWTH DIFFERENTIATION FACTOR 1; LIM KINASE 1; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SIZE; CELL SURVIVAL; CELLULAR PARAMETERS; CONTROLLED STUDY; DENDRITE COMPLEXITY; DENDRITE GROWTH; DENDRITE LENGTH; DENDRITE MORPHOLOGY; FLUORESCENCE IMAGING; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STELLATE GANGLION; SUPERIOR CERVICAL GANGLION; SYMPATHETIC NERVE CELL;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ARCHAEAL PROTEINS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CELLS, CULTURED; DENDRITES; DNA-DIRECTED DNA POLYMERASE; EMBRYO, MAMMALIAN; FLUORESCENT DYES; GANGLIA, SYMPATHETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IMAGING, THREE-DIMENSIONAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, NEUROLOGICAL; NERVE TISSUE PROTEINS; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; STATISTICS, NONPARAMETRIC; TRANSCRIPTION FACTORS;

EID: 84884174057     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4748-12.2013     Document Type: Article

References (83)

1. Anderson DJ, Carnahan JF, Michelsohn A, Patterson PH (1991) Antibody markers identify a common progenitor to sympathetic neurons and chromaffin cells in vivo and reveal the timing of commitment to neuronal differentiation in the sympathoadrenal lineage. J Neurosci 11:3507-3519. Medline
2. Ball RW, Warren-Paquin M, Tsurudome K, Liao EH, Elazzouzi F, Cavanagh C, An BS, Wang TT, White JH, Haghighi AP (2010) Retrograde BMP signaling controls synaptic growth at the NMJ by regulating trio expression in motor neurons. Neuron 66:536-549. CrossRef Medline
3. Beck HN, Drahushuk K, Jacoby DB, Higgins D, Lein PJ (2001) Bone morphogenetic protein-5 (BMP-5) promotes dendritic growth in cultured sympathetic neurons. BMC Neuroscience 2:12. CrossRef Medline
4. Brodski C, Schaubmar A, Dechant G (2002) Opposing functions of GDNF and NGF in the development of cholinergic and noradrenergic sympathetic neurons. Mol Cell Neurosci 19:528-538. CrossRef Medline
5. Büchmann-Møller S, Miescher I, John N, Krishnan J, Deng CX, Sommer L (2009) Multiple lineage-specific roles of Smad4 during neural crest development. Dev Biol 330:329-338. CrossRef Medline
6. Callahan T, Young HM, Anderson RB, Enomoto H, Anderson CR (2008) Development of satellite glia in mouse sympathetic ganglia: GDNF and GFRalpha1 are not essential. Glia 56:1428-1437. CrossRef Medline
7. Chen HL, Panchision DM (2007) Concise review: bone morphogenetic protein pleiotropism in neural stem cells and their derivatives-alternative pathways, convergent signals. Stem Cells 25:63-68. CrossRef Medline
8. Chiu CY, Kuo KK, Kuo TL, Lee KT, Cheng KH (2012) The activation of MEK/ERK signaling pathway by bone morphogenetic protein 4 to increase hepatocellular carcinoma cell proliferation and migration. Mol Cancer Res 10:415-427. CrossRef Medline
9. Darland DC, Nishi R (1998) ActivinAand follistatin influence expression of somatostatin in the ciliary ganglion in vivo. Dev Biol 202:293-303. CrossRef Medline
10. Derynck R, Zhang YE (2003) Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425:577-584. CrossRef Medline
11. Dimou L, Schnell L, Montani L, Duncan C, Simonen M, Schneider R, Liebscher T, Gullo M, Schwab ME (2006) Nogo-A-deficient mice reveal strain-dependent differences in axonal regeneration. J Neurosci 26:5591-5603. CrossRef Medline
12. Ducy P, Karsenty G (2000) The family of bone morphogenetic proteins. Kidney Int 57:2207-2214. CrossRef Medline
13. Eaton BA, Davis GW (2005) LIM Kinase1 controls synaptic stability downstream of the type IIBMP receptor. Neuron 47:695-708. CrossRef Medline
14. Ernsberger U, Patzke H, Rohrer H (1997) The developmental expression of choline acetyltransferase (ChAT) and the neuropeptide VIP in chick sympathetic neurons: evidence for different regulatory events in cholinergic differentiation. Mech Dev 68:115-126. CrossRef Medline
15. Fenstermaker V, Chen Y, Ghosh A, Yuste R (2004) Regulation of dendritic length and branching by semaphorin 3A. J Neurobiol 58:403-412. CrossRef Medline
16. Garred MM, Wang MM, Guo X, Harrington CA, Lein PJ (2011) Transcriptional responses of cultures rat sympathetic neurons during BMP-7- induced dendritic growth. PLoS One 6:e21754. CrossRef Medline
17. Gascon E, Dayer AG, Sauvain MO, Potter G, Jenny B, De Roo M, Zgraggen E, Demaurex N, Muller D, Kiss JZ (2006) GABA regulates dendritic growth by stabilizing lamellipodia in newly generated interneurons of the olfactory bulb. J Neurosci 26:12956-12966. CrossRef Medline
18. Gaudillière B, Konishi Y, de la Iglesia N, Yao GI, Bonni A (2004) A CaMKIINeuroD signaling pathway specifies dendritic morphogenesis. Neuron 41:229-241. CrossRef Medline
19. Gomes WA, Kessler JA (2001) Msx-2 and p21 mediate the pro-apoptotic but not the antiproliferative effects of BMP4 on cultured sympathetic neuroblasts. Dev Biol 237:212-221. CrossRef Medline
20. Gonsalvez DG, Cane KN, Landman KA, Enomoto H, Young HM, Anderson CR (2013) Proliferation and cell cycle dynamics in the developing stellate ganglion. J Neurosci 33:5969-5979. CrossRef Medline
21. Grueber WB, Jan LY, Jan YN (2003) Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 112:805-818. CrossRef Medline
22. Guha U, Gomes WA, Samanta J, Gupta M, Rice FL, Kessler JA (2004) Target-derived BMP signaling limits sensory neuron number and the extent of peripheral innervation in vivo. Development 131:1175-1186. CrossRef Medline
23. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Møller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sørensen FB, Vesterby A, et al. (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis 96:379-394. CrossRef Medline
24. Guo X, Wang XF (2009) Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res 19:71-88. CrossRef Medline
25. Guo X, Chandrasekaran V, Lein P, Kaplan PL, Higgins D (1999) Leukemia inhibitory factor and ciliary neurotrophic factor cause dendritic retraction in cultured rat sympathetic neurons. J Neurosci 19:2113-2121. Medline
26. Guo X, Lin Y, Horbinski C, Drahushuk KM, Kim IJ, Kaplan PL, Lein P, Wang T, Higgins D (2001) Dendritic growth induced by BMP-7 requires Smad1 and proteasome activity. J Neurobiol 48:120-130. CrossRef Medline
27. Hand R, Bortone D, Mattar P, Nguyen L, Heng JI, Guerrier S, Boutt E, Peters E, Barnes AP, Parras C, Schuurmans C, Guillemot F, Polleux F (2005) Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48:45-62. CrossRef Medline
28. Higgins D, Lein P, Osterhout D, Johnson MI (1991) Tisue culture of autonomic neurons. In: Culturing nerve cells (Banker G, Goslin K, eds), pp 177-205. Cambridge, Massachusetts: MIP.
29. Hocking JC, Hehr CL, Chang RY, Johnston J, McFarlane S (2008) TGFbeta ligands promote the initiation of retinal ganglion cell dendrites in vitro and in vivo. Mol Cell Neurosci 37:247-260. CrossRef Medline
30. Hodge LK, Klassen MP, Han BX, Yiu G, Hurrell J, Howell A, Rousseau G, Lemaigre F, Tessier-Lavigne M, Wang F (2007) Retrograde BMP signaling regulates trigeminal sensory neuron identities and the formation of precise face maps. Neuron 55:572-586. CrossRef Medline
31. Ji SJ, Jaffrey SR (2012) Intra-axonal translation of SMAD1/5/8 mediates retrograde regulation of trigeminal ganglia subtype specification. Neuron 74:95-107. CrossRef Medline
32. Jun JH, Yoon WJ, Seo SB, Woo KM, Kim GS, Ryoo HM, Baek JH (2010) BMP2-activated Erk/MAP kinase stabilizes Runx2 by increasing p300 levels and histone acetyltransferase activity. J Biol Chem 285:36410-36419. CrossRef Medline
33. Kang JS, Liu C, Derynck R (2009) New regulatory mechanisms of TGF-beta receptor function. Trends Cell Biol 19:385-394. CrossRef Medline
34. Kim IJ, Drahushuk KM, Kim WY, Gonsiorek EA, Lein P, Andres DA, Higgins D (2004) Extracellular signal-regulated kinases regulate dendritic growth in rat sympathetic neurons. J Neurosci 24:3304-3312. CrossRef Medline
35. Lee-Hoeflich ST, Causing CG, Podkowa M, Zhao X, Wrana JL, Attisano L (2004) Activation of LIMK1 by binding to the BMP receptor, BMPRII, regulates BMP-dependent dendritogenesis. EMBO J 23:4792-4801. CrossRef Medline
36. Lein P, Johnson M, Guo X, Rueger D, Higgins D (1995) Osteogenic protein-1 induces dendritic growth in rat sympathetic neurons. Neuron 15:597-605. CrossRef Medline
37. Lein PJ, Beck HN, Chandrasekaran V, Gallagher PJ, Chen HL, Lin Y, Guo X, Kaplan PL, Tiedge H, Higgins D (2002) Glia induce dendritic growth in cultured sympathetic neurons by modulating the balance between bone morphogenetic proteins (BMPs) and BMP antagonists. J Neurosci 22: 10377-10387. Medline
38. Lein PJ, Guo X, Shi GX, Moholt-Siebert M, Bruun D, Andres DA (2007) The novel GTPase Rit differentially regulates axonal and dendritic growth. J Neurosci 27:4725-4736. CrossRef Medline
39. Le Roux P, Behar S, Higgins D, Charette M (1999) OP-1 enhances dendritic growth from cerebral cortical neurons in vitro. Exp Neurol 160:151-163. CrossRef Medline
40. Liu H, Margiotta JF, Howard MJ (2005) BMP4 supports noradrenergic differentiation by a PKA-dependent mechanism. Dev Biol 286:521-536. CrossRef Medline
41. Lom B, Cohen-Cory S (1999) Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J Neurosci 19:9928-9938. Medline
42. Massagué J, Wotton D (2000) Transcriptional control by the TGF-β/Smad signaling system. EMBO J 19:1745-1754. CrossRef Medline
43. McAllister AK, Katz LC, Lo DC (1997) Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 18:767-778. CrossRef Medline
44. McPherson CE, Varley JE, Maxwell GD (2000) Expression and regulation of type IBMP receptors during early avian sympathetic ganglion development. Dev Biol 221:220-232. CrossRef Medline
45. Mishina Y, Hanks MC, Miura S, Tallquist MD, Behringer RR (2002) Generation of Bmpr/Alk3 conditional knockout mice. Genesis 32:69-72. CrossRef Medline
46. Morikawa Y, Zehir A, Maska E, Deng C, Schneider MD, Mishina Y, Cserjesi P (2009) BMP signaling regulates sympathetic nervous system development through Smad4-dependent and -independent pathways. Development 136:3575-3584. CrossRef Medline
47. Moustakas A, Heldin CH (2005) Non-Smad TGF-beta signals. J Cell Sci 118:3573-3584. CrossRef Medline
48. Otten U, Schwab M, Gagnon C, Thoenen H (1977) Selective induction of tyrosine hydroxylase and dopamine b-hydroxylase by nerve growth factor: comparison between adrenal medulla and sympathetic ganglia of adult and newborn rats. Brain Res 133:291-303. CrossRef Medline
49. Pace CJ, Tieman DG, Tieman SB (2002) Intracellular injection in fixed slices: obtaining complete dendritic arbors of large cells. J Neurosci Methods 119:23-30. CrossRef Medline
50. Parlato R, Otto C, Begus Y, Stotz S, Schütz G (2007) Specific ablation of the transcription factor CREB in sympathetic neurons surprisingly protects against developmentally regulated apoptosis. Development 134:1663-1670. CrossRef Medline
51. Pavelock KA, Girard BM, Schutz KC, Braas KM, May V (2007) Bone morphogenetic protein down-regulation of neuronal pituitary adenylate cyclase-activating polypeptide and reciprocal effects on vasoactive intestinal peptide expression. J Neurochem 100:603-616. CrossRef Medline
52. Perron JC, Dodd J (2009) ActRIIA and BMPRII type II BMP receptor subunits selectively required for Smad4-independent BMP7-evoked chemotaxis. PLoS One 4:e8198. CrossRef Medline
53. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36. CrossRef Medline
54. Podkowa M, Zhao X, Chow CW, Coffey ET, Davis RJ, Attisano L (2010) Microtubule stabilization by bone morphogenetic protein receptormediated scaffolding of c-Jun N-terminal kinase promotes dendrite formation. Mol Cell Biol 30:2241-2250. CrossRef Medline
55. Purves D, Voyvodic JT, Magrassi L, Yawo H (1987) Nerve terminal remodeling visualized in living mice by repeated examination of the same neuron. Science 238:1122-1126. CrossRef Medline
56. Reissmann E, Ernsberger U, Francis-West PH, Rueger D, Brickell PM, Rohrer H (1996) Involvement of bone morphogenetic proteins-4 and-7 in the specification of the adrenergic phenotype in developing sympathetic neurons. Development 122:2079-2088. Medline
57. Rosso SB, Sussman D, Wynshaw-Boris A, Salinas PC (2005) Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 8:34-42. CrossRef Medline
58. Rubin E (1985) Development of the rat superior cervical ganglion: ganglion cell maturation. J Neurosci 5:673-684. Medline
59. Ruit KG, Snider WD (1991) Administration or deprivation of nerve growth factor during development permanently alters neuronal geometry. J Comp Neurol 314:106-113. CrossRef Medline
60. Ruit KG, Osborne PA, Schmidt RE, Johnson EM Jr, Snider WD (1990) Nerve growth factor regulates sympathetic ganglion cell morphology and survival in the adult mouse. J Neurosci 10:2412-2419. Medline
61. Schneider C, Wicht H, Enderich J, Wegner M, Rohrer H (1999) Bone morphogenetic proteins are required in vivo for the generation of sympathetic neurons. Neuron 24:861-870. CrossRef Medline
62. Shah NM, Groves AK, Anderson DJ (1996) Alternative neural crest cell fates are instructively promoted by TGFβ superfamily members. Cell 85:331-343. CrossRef Medline
63. Sharma N, Deppmann CD, Harrington AW, St Hillaire C, Chen ZY, Lee FS, Ginty DD (2010) Long-distance control of synapse assembly by targetderived NGF. Neuron 67:422-434. CrossRef Medline
64. Sieber C, Kopf J, Hiepen C, Knaus P (2009) Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev 20:343-355. CrossRef Medline
65. Snider WD (1988) Nerve growth factor enhances dendritic arborization of sympathetic ganglion cells in developing mammals. J Neurosci 8:2628-2634. Medline
66. Stanke M, Junghans D, Geissen M, Goridis C, Ernsberger U, Rohrer H (1999) The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons. Development 126:4087-4094. Medline
67. Stanke M, Duong CV, Pape M, Geissen M, Burbach G, Deller T, Gascan H, Otto C, Parlato R, Schütz G, Rohrer H (2006) Target-dependent specification of the neurotransmitter phenotype: cholinergic differentiation of sympathetic neurons is mediated in vivo by gp130 signaling. Development 133:141-150. CrossRef Medline
68. Teitelman G, Baker H, Joh TH, Reis DJ (1979) Appearance of catecholaminesynthesizing enzymes during development of rat sympathetic nervous system: possible role of tissue environment. Proc Natl Acad SciU S A76:509-513. CrossRef Medline
69. ten Dijke P, Hill CS (2004) New insights into TGF-β-Smad signalling. Trends Biochem Sci 29:265-273. CrossRef Medline
70. Tsarovina K, Pattyn A, Stubbusch J, Mü ller F, van der Wees J, Schneider C, Brunet JF, Rohrer H (2004) Essential role of Gata transcription factors in sympathetic neuron development. Development 131:4775-4786. CrossRef Medline
71. Tsarovina K, Reiff T, Stubbusch J, Kurek D, Grosveld FG, Parlato R, Schütz G, Rohrer H (2010) The Gata3 transcription factor is required for the survival of embryonic and adult sympathetic neurons. J Neurosci 30:10833-10843. CrossRef Medline
72. Varley JE, Maxwell GD (1996) BMP-2 and BMP-4, but not BMP-6, increase the number of adrenergic cells which develop in quail trunk neural crest cultures. Exp Neurol 140:84-94. CrossRef Medline
73. Voyvodic JT (1987) Development and regulation of dendrites in the rat superior cervical ganglion. J Neurosci 7:904-912. Medline
74. Voyvodic JT (1989) Peripheral target regulation of dendritic geometry in the rat superior cervical ganglion. J Neurosci 9:1997-2010. Medline
75. Wearne SL, Rodriguez A, Ehlenberger DB, Rocher AB, Henderson SC, Hof PR (2005) New techniques for imaging, digitization and analysis of three-dimensional neural morphology on multiple scales. Neuroscience 136:661-680. CrossRef Medline
76. Withers GS, Higgins D, Charette M, Banker G (2000) Bone morphogenetic protein-7 enhances dendritic growth and receptivity to innervation in cultured hippocampal neurons. Eur J Neurosci 12:106-116. CrossRef Medline
77. Xu X, Han J, Ito Y, Bringas P Jr, Deng C, Chai Y (2008) Ectodermal Smad4 and p38 MAPK are functionally redundant in mediating TGFbeta/ BMP signaling during tooth and palate development. Dev Cell 15:322-329. CrossRef Medline
78. Yang X, Li C, Herrera PL, Deng CX (2002) Generation of Smad4/Dpc4 conditional knockout mice. Genesis 32:80-81. CrossRef Medline
79. Yawo H (1987) Changes in the dendritic geometry of mouse superior cervical ganglion cells following postganglionic axotomy. J Neurosci 7:3703-3711. Medline
80. Yi SE, Daluiski A, Pederson R, Rosen V, Lyons KM (2000) The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 127:621-630. Medline
81. Yu X, Malenka RC (2003) Beta-catenin is critical for dendritic morphogenesis. Nat Neurosci 6:1169-1177. CrossRef Medline
82. Zhang D, Mehler MF, Song Q, Kessler JA (1998) Development of bone morphogenetic protein receptors in the nervous system and possible roles in regulating trkC expression. J Neurosci 18:3314-3326. Medline
83. Zhang YE (2009) Non-Smad pathways in TGF-beta signaling. Cell Res 19: 128-139. CrossRef Medline