Lineage and stage specific requirement for Dicer1 in sympathetic ganglia and adrenal medulla formation and maintenance

Developmental Biology

Volumn 400, Issue 2, 2015, Pages 210-223

  Stubbusch, Jutta ^a   Narasimhan, Priyanka ^b   Hennchen, Melanie ^a   Huber, Katrin ^b   Unsicker, Klaus ^b   Ernsberger, Uwe ^a,c   Rohrer, Hermann ^a,c  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

Cholinergic; Chromaffin cell; Dicer1; Noradrenergic; Survival; Sympathetic neuron

Indexed keywords

MICRORNA 375; TRANSCRIPTION FACTOR MASH1; ASCL1 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DEAD BOX PROTEIN; DICER1 PROTEIN, MOUSE; RIBONUCLEASE III;

ADRENAL MEDULLA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CELL LINEAGE; CELL SURVIVAL; CHAT GENE; CHROMAFFIN CELL; CONTROLLED STUDY; DICER1 GENE; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE LOSS; GENE SILENCING; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NEUROBLAST; NEWBORN; NF M GENE; NONHUMAN; PNMT GENE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RET GENE; SIGNAL TRANSDUCTION; SYMPATHETIC GANGLION; TLX3 GENE; VACHT GENE; ANIMAL; CYTOLOGY; EMBRYOLOGY; INNERVATION; METABOLISM; NEURAL CREST; STEM CELL;

ANIMALIA; MUS;

ADRENAL MEDULLA; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL SURVIVAL; CHROMAFFIN CELLS; DEAD-BOX RNA HELICASES; GANGLIA, SYMPATHETIC; MICE; NEURAL CREST; RIBONUCLEASE III; STEM CELLS;

EID: 84929941489     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2015.01.026     Document Type: Article

References (65)

1. Abercrombie M. Estimation of nuclear population from microtome sections. Anat. Rec. 1946, 94:239-247.
2. Borges M., Linnoila R.I., Van de Velde H.J.K., Chen H., Nelkin B.D., Mabry M., Baylin S.B., Ball D.W. An achaete-scute homologue essential for neuroendocrine differentiation in the lung. Nature 1997, 386:852-855.
3. Brault V., Moore R., Kutsch S., Ishibashi M., Rowitch D.H., McMahon A.P., Sommer L., Boussadia O., Kemler R. Inactivation of the b-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001, 128:1253-1264.
4. Burau K., Stenull I., Huber K., Misawa H., Berse B., Unsicker K., Ernsberger U. c-ret regulates cholinergic properties in mouse sympathetic neurons: evidence from mutant mice. Eur. J. Neurosci. 2004, 20:353-362.
5. Chen J.A., Huang Y.P., Mazzoni E.O., Tan G.C., Zavadil J., Wichterle H. Mir-17-3p controls spinal neural progenitor patterning by regulating Olig2/Irx3 cross-repressive loop. Neuron 2011, 69:721-735.
6. Chen J.A., Wichterle H. Apoptosis of limb innervating motor neurons and erosion of motor pool identity upon lineage specific dicer inactivation. Front. Neurosci. 2012, 6:69.
7. Choi P.S., Zakhary L., Choi W.Y., Caron S., Alvarez-Saavedra E., Miska E.A., McManus M., Harfe B., Giraldez A.J., Horvitz H.R., Schier A.F., Dulac C. Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron 2008, 57:41-55.
8. Clark M.S., Lanigan T.M., Page N.M., Russo A.F. Induction of a serotonergic and neuronal phenotype in thyroid C-cells. J. Neurosci. 1995, 15:6167-6178.
9. Coupland R.E., Tomlinson A. The development and maturation of adrenal medullary chromaffin cells of the rat in vivo: a descriptive and quantitative study. Int. J. Dev. Neurosci. 1989, 7:419-438.
10. Cuellar T.L., Davis T.H., Nelson P.T., Loeb G.B., Harfe B.D., Ullian E., McManus M.T. Dicer loss in striatal neurons produces behavioral and neuroanatomical phenotypes in the absence of neurodegeneration. Proc. Natl. Acad. Sci. USA 2008, 105:5614-5619.
11. Davies A.M. Extracellular signals regulating sympathetic neuron survival and target innervation during development. Auton. Neurosci. 2009, 151:39-45.
12. Davis T.H., Cuellar T.L., Koch S.M., Barker A.J., Harfe B.D., McManus M.T., Ullian E.M. Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J. Neurosci. 2008, 28:4322-4330.
13. Deneris E.S., Hobert O. Maintenance of postmitotic neuronal cell identity. Nat. Neurosci. 2014, 17:899-907.
14. Enomoto H., Crawford P.A., Gorodinsky A., Heuckeroth R.O., Johnson E.M., Milbrandt J. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 2001, 128:3963-3974.
15. Ernsberger U., Patzke H., Rohrer H. 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. 1997, 68:115-126.
16. Fagan A.M., Zhang H., Landis S., Smeyne R.J., Silos-Santiago I., Barbacid M. TrkA, but not TrkC, receptors are essential for survival of sympathetic neurons in vivo. J. Neurosci. 1996, 16:6208-6218.
17. Francis N., Farinas I., Brennan C., Rivas-Plata K., Backus C., Reichardt L., Landis S. NT-3, like NGF, is required for survival of sympathetic neurons, but not their precursors. Dev. Biol. 1999, 210:411-427.
18. Furlan A., Lubke M., Adameyko I., Lallemend F., Ernfors P. The transcription factor Hmx1 and growth factor receptor activities control sympathetic neurons diversification. EMBO J. 2013, 32:1613-1625.
19. Georgi S.A., Reh T.A. Dicer is required for the transition from early to late progenitor state in the developing mouse retina. J. Neurosci. 2010, 30:4048-4061.
20. Gonsalvez D.G., Cane K.N., Landman K.A., Enomoto H., Young H.M., Anderson C.R. Proliferation and cell cycle dynamics in the developing stellate ganglion. J. Neurosci. 2013, 33:5969-5979.
21. Guillemot F., Joyner A.L. Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system. Mech. Dev. 1993, 42:171-185.
22. Guillemot F., Lo L.-C., Johnson J.E., Auerbach A., Anderson D.J., Joyner A.L. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 1993, 75:463-476.
23. Gundersen H.J., Bendtsen T.F., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988, 96:379-394.
24. Haramati S., Navon I., Issler O., Ezra-Nevo G., Gil S., Zwang R., Hornstein E., Chen A. MicroRNA as repressors of stress-induced anxiety: the case of amygdalar miR-34. J. Neurosci. 2011, 31:14191-14203.
25. Harfe B.D., McManus M.T., Mansfield J.H., Hornstein E., Tabin C.J. The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc. Natl. Acad. Sci. USA 2005, 102:10898-10903.
26. Hong S.J., Huh Y.H., Leung A., Choi H.J., Ding Y., Kang U.J., Yoo S.H., Buettner R., Kim K.S. Transcription factor AP-2beta regulates the neurotransmitter phenotype and maturation of chromaffin cells. Mol. Cell. Neurosci. 2011, 46:245-251.
27. Howard M.J., Stanke M., Schneider C., Wu X., Rohrer H. The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification. Development 2000, 127:4073-4081.
28. Huang T., Hu J., Wang B., Nie Y., Geng J., Cheng L. Tlx3 controls cholinergic transmitter and Peptide phenotypes in a subset of prenatal sympathetic neurons. J. Neurosci. 2013, 33:10667-10675.
29. Huang T., Liu Y., Huang M., Zhao X., Cheng L. Wnt1-cre-mediated conditional loss of Dicer results in malformation of the midbrain and cerebellum and failure of neural crest and dopaminergic differentiation in mice. J. Mol. Cell Biol. 2010, 2:152-163.
30. Huber K. The sympathoadrenal cell lineage: specification, diversification, and new perspectives. Dev. Biol. 2006, 298:335-343.
31. Huber K., Bruhl B., Guillemot F., Olson E.N., Unsicker K. Development of chromaffin cells depends on MASH1 function. Development 2002, 129:4729-4738.
32. Huber K., Kalcheim C., Unsicker K. The development of the chromaffin cell lineage from the neural crest. Auton. Neurosci. 2009, 151:10-16.
33. Huber K., Karch N., Ernsberger U., Goridis G., Unsicker K. The role of Phox2B in chromaffin cell development. Dev. Biol. 2005, 279:501-508.
34. Huber K., Narasimhan P., Shtukmaster S., Pfeifer D., Evans S.M., Sun Y. The LIM-Homeodomain transcription factor Islet-1 is required for the development of sympathetic neurons and adrenal chromaffin cells. Dev. Biol. 2013, 380:286-298.
35. Jurecka W., Lassman H., Horander H. The proliferation of adrenal medullary cells in newborn and adult mice. Cell Tissue Res. 1978, 189:305-312.
36. Kadkhodaei B., Ito T., Joodmardi E., Mattsson B., Rouillard C., Carta M., Muramatsu S., Sumi-Ichinose C., Nomura T., Metzger D., Chambon P., Lindqvist E., Larsson N.G., Olson L., Bjorklund A., Ichinose H., Perlmann T. Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons. J. Neurosci. 2009, 29:15923-15932.
37. Konopka W., Kiryk A., Novak M., Herwerth M., Parkitna J.R., Wawrzyniak M., Kowarsch A., Michaluk P., Dzwonek J., Arnsperger T., Wilczynski G., Merkenschlager M., Theis F.J., Kohr G., Kaczmarek L., Schutz G. MicroRNA loss enhances learning and memory in mice. J. Neurosci. 2010, 30:14835-14842.
38. Lanigan T.M., DeRaad S.K., Russo A.F. Requirement of the MASH-1 transcription factor for neuroendocrine differentiation of thyroid C cells. J. Neurobiol. 1998, 34:126-134.
39. Majdazari A., Stubbusch J., Muller C.M., Hennchen M., Weber M., Deng C.X., Mishina Y., Schutz G., Deller T., Rohrer H. Dendrite complexity of sympathetic neurons is controlled during postnatal development by BMP signaling. J. Neurosci. 2013, 33:15132-15144.
40. Nikoletopoulou V., Lickert H., Frade J.M., Rencurel C., Giallonardo P., Zhang L., Bibel M., Barde Y.A. Neurotrophin receptors TrkA and TrkC cause neuronal death whereas TrkB does not. Nature 2010, 467:59-63.
41. Nishikawa E., Osada H., Okazaki Y., Arima C., Tomida S., Tatematsu Y., Taguchi A., Shimada Y., Yanagisawa K., Yatabe Y., Toyokuni S., Sekido Y., Takahashi T. miR-375 is activated by ASH1 and inhibits YAP1 in a lineage-dependent manner in lung cancer. Cancer Res. 2011, 71:6165-6173.
42. Osada H., Tomida S., Yatabe Y., Tatematsu Y., Takeuchi T., Murakami H., Kondo Y., Sekido Y., Takahashi T. Roles of achaete-scute homologue 1 in DKK1 and E-cadherin repression and neuroendocrine differentiation in lung cancer. Cancer Res. 2008, 68:1647-1655.
43. Parlato R., Otto C., Begus Y., Stotz S., Schutz G. Specific ablation of the transcription factor CREB in sympathetic neurons surprisingly protects against developmentally regulated apoptosis. Development 2007, 134:1663-1670.
44. Parlato R., Otto C., Tuckermann J., Stotz S., Kaden S., Grone H.J., Unsicker K., Schutz G. Conditional inactivation of glucocorticoid receptor gene in dopamine-beta-hydroxylase cells impairs chromaffin cell survival. Endocrinology 2009, 150:1775-1781.
45. Pattyn A., Guillemot F., Brunet J.F. Delays in neuronal differentiation in Mash1/Ascl1 mutants. Dev. Biol. 2006, 295:67-75.
46. Pattyn A., Morin X., Cremer H., Goridis C., Brunet J.-F. The homeobox gene Phox2b is essential for the development of all autonomic derivatives of the neural crest. Nature 1999, 399:366-370.
47. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002, 30:e36.
48. Potzner M.R., Tsarovina K., Binder E., Penzo-Mendez A., Lefebvre V., Rohrer H., Wegner M., Sock E. Sequential requirement of Sox4 and Sox11 during development of the sympathetic nervous system. Development 2010, 137:775-784.
49. Poy M.N., Hausser J., Trajkovski M., Braun M., Collins S., Rorsman P., Zavolan M., Stoffel M. miR-375 maintains normal pancreatic alpha- and beta-cell mass. Proc. Natl. Acad. Sci. USA 2009, 106:5813-5818.
50. Rohrer H., Acheson A.L., Thibault J., Thoenen H. Developmental potential of quail dorsal root ganglion cells analyzed in vitro and in vivo. J. Neurosci. 1986, 6:2616-2624.
51. Ruit K.G., Osborne P.A., Schmidt R.E., Johnson E.M., Snider W.D. Nerve growth factor regulates sympathetic ganglion cell morphology and survival in the adult mouse. J. Neurosci. 1990, 10:2412-2419.
52. Schaefer A., O'Carroll D., Tan C.L., Hillman D., Sugimori M., Llinas R., Greengard P. Cerebellar neurodegeneration in the absence of microRNAs. J. Exp. Med. 2007, 204:1553-1558.
53. Schmidt M., Huber L., Majdazari A., Schutz G., Williams T., Rohrer H. The transcription factors AP-2beta and AP-2alpha are required for survival of sympathetic progenitors and differentiated sympathetic neurons. Dev. Biol. 2011, 355:89-100.
54. Schober A., Minichiello L., Keller M., Huber K., Layer P.G., Roig-López J.L., García-Arrarás J.E., Klein R., Unsicker K. Reduced acetylcholinesterase (AChE) activity in adrenal medulla and loss of sympathetic preganglionic neurons in TrkA-deficient, but not TrkB-deficient, mice. J. Neurosci. 1997, 17:891-903.
55. Shtukmaster S., Schier M.C., Huber K., Krispin S., Kalcheim C., Unsicker K. Sympathetic neurons and chromaffin cells share a common progenitor in the neural crest in vivo. Neural Dev. 2013, 8:12.
56. Stanke M., Duong C.V., Pape M., Geissen M., Burbach G., Deller T., Gascan H., Otto C., Parlato R., Schütz G., Rohrer H. Target-dependent specification of the neurotransmitter phenotype: cholinergic differentiation of sympathetic neurons is mediated in vivo by gp130 signaling. Development 2006, 133:141-150.
57. Stanke M., Geissen M., Götz R., Ernsberger U., Rohrer H. The early expression of VAChT and VIP in mouse sympathetic ganglia is not induced by cytokines acting through LIFRb or CNTFRa. Mech. Dev. 2000, 91:91-96.
58. Stubbusch J., Narasimhan P., Huber K., Unsicker K., Rohrer H., Ernsberger U. Synaptic protein and pan-neuronal gene expression and their regulation by Dicer-dependent mechanisms differ between neurons and neuroendocrine cells. Neural Dev. 2013, 8:16.
59. Theiler K. The House Mouse: Atlas of Embryonic Development 1989, Springer-Verlag, New York.
60. Tischler A.S. Cell proliferation in the adult adrenal medulla: chromaffin cells as a model for indirect carcinogenesis. Endocrine System 1996, 405-411. Springer-Verlag, Berlin, Heidelberg. T.C. Jones (Ed.).
61. Tsarovina K., Pattyn A., Stubbusch J., Müller F., Van der Wees J., Schneider C., Brunet J.F., Rohrer H. Essential role of Gata transcription factors in sympathetic neuron development. Development 2004, 131:4775-4786.
62. Tsarovina K., Reiff T., Stubbusch J., Kurek D., Grosveld F.G., Parlato R., Schutz G., Rohrer H. The Gata3 transcription factor is required for the survival of embryonic and adult sympathetic neurons. J. Neurosci. 2010, 30:10833-10843.
63. VanDusen N.J., Vincentz J.W., Firulli B.A., Howard M.J., Rubart M., Firulli A.B. Loss of Hand2 in a population of Periostin lineage cells results in pronounced bradycardia and neonatal death. Dev. Biol. 2014, 388:149-158.
64. Wildner H., Gierl M.S., Strehle M., Pla P., Birchmeier C. Insm1 (IA-1) is a crucial component of the transcriptional network that controls differentiation of the sympatho-adrenal lineage. Development 2008, 135:473-481.
65. Zehir A., Hua L.L., Maska E.L., Morikawa Y., Cserjesi P. Dicer is required for survival of differentiating neural crest cells. Dev. Biol. 2010, 340:459-467.