Target-dependent inhibition of sympathetic neuron growth via modulation of a BMP signaling pathway

Developmental Biology

Volumn 315, Issue 2, 2008, Pages 404-417

  Moon, Jung Il ^a   Birren, Susan J ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

Basic helix loop helix transcription factor; Bone morphogenetic protein; Cardiac myocyte; Matrix Gla protein; Microarray; Sympathetic neuron; Target contact

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; HELIX LOOP HELIX PROTEIN; OSTEOCALCIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR SYSTEM; CELL MATURATION; CELL SURVIVAL; EMBRYO; GENE EXPRESSION; HEART MUSCLE CELL; MICROARRAY ANALYSIS; NERVE FIBER GROWTH; NERVE GROWTH; NEUROFILAMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYMPATHETIC NERVE;

EID: 39949084472     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.12.041     Document Type: Article

References (73)

1. D.H. Baird M.E. Hatten C.A. Mason Cerebellar target neurons provide a stop signal for afferent neurite extension in vitro J. Neurosci. 12 1992 619 634
2. D.H. Baird E. Trenkner C.A. Mason Arrest of afferent axon extension by target neurons in vitro is regulated by the NMDA receptor J. Neurosci. 16 1996 2642 2648
3. H.N. Beck K. Drahushuk D.B. Jacoby D. Higgins P.J. Lein Bone morphogenetic protein-5 (BMP-5) promotes dendritic growth in cultured sympathetic neurons BMC Neurosci. 2 2001 12
4. S. Bharmal J.D. Slonimsky J.N. Mead C.P. Sampson A.M. Tolkovsky B. Yang R. Bargman S.J. Birren Target cells promote the development and functional maturation of neurons derived from a sympathetic precursor cell line Dev. Neurosci. 23 2001 153 164
5. K. Bostrom D. Tsao S. Shen Y. Wang L.L. Demer Matrix GLA protein modulates differentiation induced by bone morphogenetic protein-2 in C3H10T1/2 cells J. Biol. Chem. 276 2001 14044 14052
6. M.A. Bounpheng T.A. Morrish S.G. Dodds B.A. Christy Negative regulation of selected bHLH proteins by eHAND Exp. Cell Res. 257 2000 320 331
7. I. Carrio Cardiac neurotransmission imaging J. Nucl. Med. 42 2001 1062 1076
8. A. Chalazonitis F. D'Autreaux U. Guha T.D. Pham C. Faure J.J. Chen D. Roman L. Kan T.P. Rothman J.A. Kessler M.D. Gershon Bone morphogenetic protein-2 and -4 limit the number of enteric neurons but promote development of a TrkC-expressing neurotrophin-3-dependent subset J. Neurosci. 24 2004 4266 4282
9. L.L. Chun P.H. Patterson Role of nerve growth factor in the development of rat sympathetic neurons in vitro: I. Survival, growth, and differentiation of catecholamine production J. Cell. Biol. 75 1977 694 704
10. L. Conforti N. Tohse N. Sperelakis Influence of sympathetic innervation on the membrane electrical properties of neonatal rat cardiomyocytes in culture J. Dev. Physiol. 15 1991 237 246
11. T. Cowen C. Thrasivoulou S.A. Shaw T.A. Abdel-Rahman Transplanted sweat glands from mature and aged donors determine cholinergic phenotype and altered density of host sympathetic nerves J. Auton. Nerv. Syst. 58 1996 153 162
12. Y.S. Dai P. Cserjesi The basic helix–loop–helix factor, HAND2, functions as a transcriptional activator by binding to E-boxes as a heterodimer J. Biol. Chem. 277 2002 12604 12612
13. A. Del Signore V. De Sanctis E. Di Mauro R. Negri C. Perrone-Capano P. Paggi Gene expression pathways induced by axotomy and decentralization of rat superior cervical ganglion neurons Eur. J. Neurosci. 23 2006 65 74
14. A. Dimitropoulou J.L. Bixby Motor neurite outgrowth is selectively inhibited by cell surface MuSK and agrin Mol. Cell. Neurosci. 28 2005 292 302
15. J.J. Dore K.L. Crotty S.J. Birren Inhibition of glial maturation by bone morphogenetic protein 2 in a neural crest-derived cell line Dev. Neurosci. 27 2005 37 48
16. U. Ernsberger E. Reissmann I. Mason H. Rohrer The expression of dopamine beta-hydroxylase, tyrosine hydroxylase, and Phox2 transcription factors in sympathetic neurons: evidence for common regulation during noradrenergic induction and diverging regulation later in development Mech. Dev. 92 2000 169 177
17. C. Faure A. Chalazonitis C. Rheaume G. Bouchard S.G. Sampathkumar K.J. Yarema M.D. Gershon Gangliogenesis in the enteric nervous system: roles of the polysialylation of the neural cell adhesion molecule and its regulation by bone morphogenetic protein-4 Dev. Dyn. 236 2007 (spc1)
18. B.A. Firulli D.B. Hadzic J.R. McDaid A.B. Firulli The basic helix–loop–helix transcription factors dHAND and eHAND exhibit dimerization characteristics that suggest complex regulation of function J. Biol. Chem. 275 2000 33567 33573
19. B.A. Firulli M.J. Howard J.R. McDaid L. McIlreavey K.M. Dionne V.E. Centonze P. Cserjesi D.M. Virshup A.B. Firulli PKA, PKC, and the protein phosphatase 2A influence HAND factor function: a mechanism for tissue-specific transcriptional regulation Mol. Cell 12 2003 1225 1237
20. M. Fu B.P. Vohra D. Wind R.O. Heuckeroth BMP signaling regulates murine enteric nervous system precursor migration, neurite fasciculation, and patterning via altered Ncam1 polysialic acid addition Dev. Biol. 299 2006 137 150
21. J. Gingras S. Rassadi E. Cooper M. Ferns Agrin plays an organizing role in the formation of sympathetic synapses J. Cell Biol. 158 2002 1109 1118
22. X. Guo D. Rueger D. Higgins Osteogenic protein-1 and related bone morphogenetic proteins regulate dendritic growth and the expression of microtubule-associated protein-2 in rat sympathetic neurons Neurosci. Lett. 245 1998 131 134
23. G. Haase E. Dessaud A. Garces B. de Bovis M. Birling P. Filippi H. Schmalbruch S. Arber O. deLapeyriere GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools Neuron 35 2002 893 905
24. P.V. Hauschka J.B. Lian D.E. Cole C.M. Gundberg Osteocalcin and matrix Gla protein: vitamin K-dependent proteins in bone Physiol. Rev. 69 1989 990 1047
25. A.A. Hill P.R. Riley Differential regulation of Hand1 homodimer and Hand1-E12 heterodimer activity by the cofactor FHL2 Mol. Cell. Biol. 24 2004 9835 9847
26. C. Horbinski E.K. Stachowiak V. Chandrasekaran E. Miuzukoshi D. Higgins M.K. Stachowiak Bone morphogenetic protein-7 stimulates initial dendritic growth in sympathetic neurons through an intracellular fibroblast growth factor signaling pathway J. Neurochem. 80 2002 54 63
27. M. Howard D.N. Foster P. Cserjesi Expression of HAND gene products may be sufficient for the differentiation of avian neural crest-derived cells into catecholaminergic neurons in culture Dev. Biol. 215 1999 62 77
28. M.J. Howard M. Stanke C. Schneider X. Wu H. Rohrer The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification Development 127 2000 4073 4081
29. F. Ledda G. Paratcha C.F. Ibanez Target-derived GFRalpha1 as an attractive guidance signal for developing sensory and sympathetic axons via activation of Cdk5 Neuron 36 2002 387 401
30. P. Lein M. Johnson X. Guo D. Rueger D. Higgins Osteogenic protein-1 induces dendritic growth in rat sympathetic neurons Neuron 15 1995 597 605
31. P.J. Lein H.N. Beck V. Chandrasekaran P.J. Gallagher H.L. Chen Y. Lin X. Guo P.L. Kaplan H. Tiedge D. Higgins Glia induce dendritic growth in cultured sympathetic neurons by modulating the balance between bone morphogenetic proteins (BMPs) and BMP antagonists J. Neurosci. 22 2002 10377 10387
32. R. Levi-Montalcini P.U. Angeletti Essential role of the nerve growth factor in the survival and maintenance of dissociated sensory and sympathetic embryonic nerve cells in vitro Dev. Biol. 7 1963 653 659
33. C. Li W.H. Wong Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection Proc. Natl. Acad. Sci. U. S. A. 98 2001 31 36
34. K.J. Livak T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(− Delta Delta C (T)) method Methods 25 2001 402 408
35. S.T. Lockhart J.N. Mead J.M. Pisano J.D. Slonimsky S.J. Birren Nerve growth factor collaborates with myocyte-derived factors to promote development of presynaptic sites in cultured sympathetic neurons J. Neurobiol. 42 2000 460 476
36. S.T. Lockhart G.G. Turrigiano S.J. Birren Nerve growth factor modulates synaptic transmission between sympathetic neurons and cardiac myocytes J. Neurosci. 17 1997 9573 9582
37. M.E. Lucas F. Muller R. Rudiger P.D. Henion H. Rohrer The bHLH transcription factor hand2 is essential for noradrenergic differentiation of sympathetic neurons Development 133 2006 4015 4024
38. F. Mann C. Peuckert F. Dehner R. Zhou J. Bolz Ephrins regulate the formation of terminal axonal arbors during the development of thalamocortical projections Development 129 2002 3945 3955
39. M.C. Manzini M.S. Ward Q. Zhang M.D. Lieberman C.A. Mason The stop signal revised: immature cerebellar granule neurons in the external germinal layer arrest pontine mossy fiber growth J. Neurosci. 26 2006 6040 6051
40. C.A. Mason M.E. Morrison M.S. Ward Q. Zhang D.H. Baird Axon–target interactions in the developing cerebellum Perspect. Dev. Neurobiol. 5 1997 69 82
41. M.F. Mehler P.C. Mabie G. Zhu S. Gokhan J.A. Kessler Developmental changes in progenitor cell responsiveness to bone morphogenetic proteins differentially modulate progressive CNS lineage fate Dev. Neurosci. 22 2000 74 85
42. Y. Morikawa F. D'Autreaux M.D. Gershon P. Cserjesi Hand2 determines the noradrenergic phenotype in the mouse sympathetic nervous system Dev. Biol. 307 2007 114 126
43. M. Murshed T. Schinke M.D. McKee G. Karsenty Extracellular matrix mineralization is regulated locally; different roles of two Gla-containing proteins J. Cell Biol. 165 2004 625 630
44. A. Nobin B. Falck S. Ingemansson J. Jarhult E. Rosengren Organization and function of the sympathetic innervation Acta Physiol. Scand., Suppl. 452 1977 103 106
45. P.H. O'Lague D.D. Potter E.J. Furshpan Studies on rat sympathetic neurons developing in cell culture: I. Growth characteristics and electrophysiological properties Dev. Biol. 67 1978 384 403
46. D.D. O'Leary C.D. Heffner L. Kutka L. Lopez-Mascaraque A. Missias B.S. Reinoso A target-derived chemoattractant controls the development of the corticopontine projection by a novel mechanism of axon targeting Development Suppl. 2 1991 123 130
47. D.M. Panchision J.M. Pickel L. Studer S.H. Lee P.A. Turner T.G. Hazel R.D. McKay Sequential actions of BMP receptors control neural precursor cell production and fate Genes Dev. 15 2001 2094 2110
48. J.M. Pisano S.J. Birren Restriction of developmental potential during divergence of the enteric and sympathetic neuronal lineages Development 126 1999 2855 2868
49. J.M. Pisano F. Colon-Hastings S.J. Birren Postmigratory enteric and sympathetic neural precursors share common, developmentally regulated, responses to BMP2 Dev. Biol. 227 2000 1 11
50. B.E. Porter J. Weis J.R. Sanes A motoneuron-selective stop signal in the synaptic protein S-laminin Neuron 14 1995 549 559
51. E. Reissmann U. Ernsberger P.H. Francis-West D. Rueger P.M. Brickell H. Rohrer Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons Development 122 1996 2079 2088
52. V. Rowe J. Parr Pineal cells enhance choline acetyltransferase activity in sympathetic neurons J. Neurobiol. 11 1980 547 556
53. E. Rubin Development of the rat superior cervical ganglion: ingrowth of preganglionic axons J. Neurosci. 5 1985 685 696
54. E. Rubin Development of the rat superior cervical ganglion: initial stages of synapse formation J. Neurosci. 5 1985 697 704
55. A.A. Sarkar M.J. Howard Perspectives on integration of cell extrinsic and cell intrinsic pathways of signaling required for differentiation of noradrenergic sympathetic ganglion neurons Auton. Neurosci. 126–127 2006 225 231
56. C. Schneider H. Wicht J. Enderich M. Wegner H. Rohrer Bone morphogenetic proteins are required in vivo for the generation of sympathetic neurons Neuron 24 1999 861 870
57. R. Schotzinger X. Yin S. Landis Target determination of neurotransmitter phenotype in sympathetic neurons J. Neurobiol. 25 1994 620 639
58. N.M. Shah A.K. Groves D.J. Anderson Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members Cell 85 1996 331 343
59. T. Shiga M. Lustig M. Grumet T. Shirai Cell adhesion molecules regulate guidance of dorsal root ganglion axons in the marginal zone and their invasion into the mantle layer of embryonic spinal cord Dev. Biol. 192 1997 136 148
60. J. Shou R.C. Murray P.C. Rim A.L. Calof Opposing effects of bone morphogenetic proteins on neuron production and survival in the olfactory receptor neuron lineage Development 127 2000 5403 5413
61. J.D. Slonimsky B. Yang J.M. Hinterneder E.B. Nokes S.J. Birren BDNF and CNTF regulate cholinergic properties of sympathetic neurons through independent mechanisms Mol. Cell. Neurosci. 23 2003 648 660
62. J.D. Slonimsky M.D. Mattaliano J.I. Moon L.C. Griffith S.J. Birren Role for calcium/calmodulin-dependent protein kinase II in the p75-mediated regulation of sympathetic cholinergic transmission Proc. Natl. Acad. Sci. U. S. A. 103 2006 2915 2919
63. W.D. Snider Nerve growth factor enhances dendritic arborization of sympathetic ganglion cells in developing mammals J. Neurosci. 8 1988 2628 2634
64. L.M. Stevens S.C. Landis Developmental interactions between sweat glands and the sympathetic neurons which innervate them: effects of delayed innervation on neurotransmitter plasticity and gland maturation Dev. Biol. 130 1988 703 720
65. T. Taniwaki J.P. Schwartz Somatostatin enhances neurofilament expression and neurite outgrowth in cultured rat cerebellar granule cells Brain Res. Dev. Brain Res. 88 1995 109 116
66. J.T. Voyvodic Development and regulation of dendrites in the rat superior cervical ganglion J. Neurosci. 7 1987 904 912
67. R. Wallin D. Cain S.M. Hutson D.C. Sane R. Loeser Modulation of the binding of matrix Gla protein (MGP) to bone morphogenetic protein-2 (BMP-2) Thromb. Haemost. 84 2000 1039 1044
68. X. Wu M.J. Howard Transcripts encoding HAND genes are differentially expressed and regulated by BMP4 and GDNF in developing avian gut Gene Expr. 10 2002 279 293
69. X.M. Xu D.A. Fisher L. Zhou F.A. White S. Ng W.D. Snider Y. Luo The transmembrane protein semaphorin 6A repels embryonic sympathetic axons J. Neurosci. 20 2000 2638 2648
70. T. Yabe I. Samuels J.P. Schwartz Bone morphogenetic proteins BMP-6 and BMP-7 have differential effects on survival and neurite outgrowth of cerebellar granule cell neurons J. Neurosci. Res. 68 2002 161 168
71. H. Yawo Changes in the dendritic geometry of mouse superior cervical ganglion cells following postganglionic axotomy J. Neurosci. 7 1987 3703 3711
72. A.F. Zebboudj M. Imura K. Bostrom Matrix GLA protein, a regulatory protein for bone morphogenetic protein-2 J. Biol. Chem. 277 2002 4388 4394
73. Q. Zhang C.A. Mason Developmental regulation of mossy fiber afferent interactions with target granule cells Dev. Biol. 195 1998 75 87