Abstract
Neuronal connectivity is dependent on size and shape of the dendritic arbor. However, mechanisms controlling dendritic arborization, especially in the peripheral nervous system, are not completely understood. Previous studies have shown that bone morphogenetic proteins (BMPs) are important initiators of dendritic growth in peripheral neurons. In this study, we examined the hypothesis that post-transcriptional regulation mediated by microRNAs (miRNAs) is necessary for BMP-7-induced dendritic growth in these neurons. To examine the role of miRNAs in BMP-7-induced dendritic growth, microarray analyses was used to profile miRNA expression in cultured sympathetic neurons from the superior cervical ganglia of embryonic day 21 rat pups at 6 and 24 h after treatment with BMP-7 (50 ng/mL). Our data showed that BMP-7 significantly regulated the expression of 43 of the 762 miRNAs. Of the 43 miRNAs, 22 showed robust gene expression; 14 were upregulated by BMP-7 and 8 were downregulated by BMP-7. The expression profile for miR-335, miR-664-1*, miR-21, and miR-23b was confirmed using qPCR analyses. Functional studies using morphometric analyses of dendritic growth in cultured sympathetic neurons transfected with miRNA mimics and inhibitors indicated that miR-664-1*, miR-23b, and miR-21 regulated early stages of BMP-7-induced dendritic growth. In summary, our data provide evidence for miRNA-mediated post-transcriptional regulation as important downstream component of BMP-7 signaling during early stages of dendritic growth in sympathetic neurons.
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References
Ahmed MI, Mardaryev AN, Lewis CJ et al (2011) MicroRNA-21 is an important downstream component of BMP signalling in epidermal keratinocytes. J Cell Sci 124:3399–3404
Bicker S, Lackinger M, Weiß K, Schratt G (2014) MicroRNA-132, -134, and -138: a microRNA troika rules in neuronal dendrites. Cell Mol Life Sci. https://doi.org/10.1007/s00018-014-1671-7
Boivin GP, Hickman DL, Creamer-Hente MA et al (2017) Review of CO2 as a Euthanasia agent for laboratory rats and mice. J Am Assoc Lab Anim Sci 56:491–499
Bruckenstein DA, Higgins D (1988) Morphological differentiation of embryonic rat sympathetic neurons in tissue culture. Dev Biol 128:337–348. https://doi.org/10.1016/0012-1606(88)90296-5
Caceres A, Banker G, Steward O et al (1984) MAP2 is localized to the dendrites of hippocampal neurons which develop in culture. Brain Res 315:314–318
Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655. https://doi.org/10.1016/j.cell.2009.01.035
Chandrasekaran V, Lea C, Sosa JC et al (2015) Reactive oxygen species are involved in BMP-induced dendritic growth in cultured rat sympathetic neurons. Mol Cell Neurosci 67:116–125. https://doi.org/10.1016/j.mcn.2015.06.007
Chen Y, Gelfond JAL, McManus LM, Shireman PK (2009) Reproducibility of quantitative RT-PCR array in miRNA expression profiling and comparison with microarray analysis. BMC Genom 10:407. https://doi.org/10.1186/1471-2164-10-407
Chen Q, Qiu F, Zhou K et al (2017a) Pathogenic role of microRNA-21 in diabetic retinopathy through downregulation of PPARα. Diabetes 66:1671–1682. https://doi.org/10.2337/db16-1246
Chen X, Jiang X-M, Zhao L-J et al (2017b) MicroRNA-195 prevents dendritic degeneration and neuron death in rats following chronic brain hypoperfusion. Cell Death Dis 8:e2850. https://doi.org/10.1038/cddis.2017.243
Comery TA, Harris JB, Willems PJ et al (1997) Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc Natl Acad Sci USA 94:5401–5404
Copf T (2016) Impairments in dendrite morphogenesis as etiology for neurodevelopmental disorders and implications for therapeutic treatments. Neurosci Biobehav Rev 68:946–978. https://doi.org/10.1016/J.NEUBIOREV.2016.04.008
Davies DC (1978) Neuronal numbers in the superior cervical ganglion of the neonatal rat. J Anat 127:43–51
Davis TH, Cuellar TL, Koch SM et al (2008) Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J Neurosci 28:4322–4330. https://doi.org/10.1523/JNEUROSCI.4815-07.2008
Davis BN, Hilyard AC, Nguyen PH et al (2010) Smad proteins bind a conserved RNA sequence to promote microRNA maturation by Drosha. Mol Cell 39:373–384
De Castro F, Sánchez-Vives MV, Muñoz-Martínez EJ, Gallego R (1995) Effects of postganglionic nerve section on synaptic transmission in the superior cervical ganglion of the guinea-pig. Neuroscience 67:689–695. https://doi.org/10.1016/0306-4522(95)00079-X
De Pablo-Fernandez E, Tur C, Revesz T et al (2017) Association of autonomic dysfunction with disease progression and survival in Parkinson disease. JAMA Neurol 74:970. https://doi.org/10.1001/jamaneurol.2017.1125
De Santi C, Vencken S, Blake J et al (2017) Identification of MiR-21-5p as a functional regulator of mesothelin expression using MicroRNA capture affinity coupled with next generation sequencing. PLoS ONE 12:e0170999. https://doi.org/10.1371/journal.pone.0170999
Diotel N, Beil T, Strähle U, Rastegar S (2015) Differential expression of id genes and their potential regulator znf238 in zebrafish adult neural progenitor cells and neurons suggests distinct functions in adult neurogenesis. Gene Expr Patterns 19:1–13. https://doi.org/10.1016/j.gep.2015.05.004
Dorval V, Smith PY, Delay C et al (2012) Gene network and pathway analysis of mice with conditional ablation of Dicer in post-mitotic neurons. PLoS ONE 7:e44060. https://doi.org/10.1371/journal.pone.0044060
Drahushuk K, Connell TD, Higgins D (2002) Pituitary adenylate cyclase-activating polypeptide and vasoactive intestinal peptide inhibit dendritic growth in cultured sympathetic neurons. J Neurosci 22:6560–6569
Du J, Yang S, An D et al (2009) BMP-6 inhibits microRNA-21 expression in breast cancer through repressing delta EF1 and AP-1. Cell Res 19:487–496
Fay MJ, Alt LAC, Ryba D et al (2018) Cadmium nephrotoxicity is associated with altered MicroRNA expression in the rat renal cortex. Toxics 6:16. https://doi.org/10.3390/toxics6010016
Feng J, Liang Y, Wang F, Chen J (2013) Detection of genetically modified tomato using PCR coupled with muParaflo microfluidics microarrays. J Nanosci Nanotechnol 13:8266–8274
Garey L (2010) When cortical development goes wrong: schizophrenia as a neurodevelopmental disease of microcircuits. J Anat 217:324–333. https://doi.org/10.1111/j.1469-7580.2010.01231.x
Garred MM, Wang MM, Guo X et al (2011) Transcriptional responses of cultured rat sympathetic neurons during BMP-7-induced dendritic growth. PLoS ONE 6:e21754
Ge X, Zheng L, Huang M et al (2015) MicroRNA expression profiles associated with acquired gefitinib-resistance in human lung adenocarcinoma cells. Mol Med Rep 11:333–340. https://doi.org/10.3892/mmr.2014.2757
Ghogha A, Bruun DA, Lein PJ (2012) Inducing dendritic growth in cultured sympathetic neurons. J Vis Exp 61:e3546
Guo X, Metzler-Northrup J, Lein P et al (1997) Leukemia inhibitory factor and ciliary neurotrophic factor regulate dendritic growth in cultures of rat sympathetic neurons. Dev Brain Res 104:101–110. https://doi.org/10.1016/S0165-3806(97)00142-9
Guo X, Chandrasekaran V, Lein P et al (1999) Leukemia inhibitory factor and ciliary neurotrophic factor cause dendritic retraction in cultured rat sympathetic neurons. J Neurosci 19:2113–2121. https://doi.org/10.1523/JNEUROSCI.19-06-02113.1999
Guo X, Lin Y, Horbinski C et al (2001) Dendritic growth induced by BMP-7 requires Smad1 and proteasome activity. J Neurobiol 48:120–130
Hackbarth H, Küppers N, Bohnet W (2000) Euthanasia of rats with carbon dioxide-animal welfare aspects. Lab Anim 34:91–96. https://doi.org/10.1258/002367700780578055
Harada A, Teng J, Takei Y et al (2002) MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol 158:541–549. https://doi.org/10.1083/jcb.200110134
Higgins D, Lein P, Osterhout DJ, Johnson M (1991) Tissue culture of autonomic neurons. In: Banker G, Goslin K (eds) Culturing nerve cells. MIT Press, Cambridge, pp 177–205
Higgins D, Burack M, Lein P, Banker G (1997) Mechanisms of neuronal polarity. Curr Opin Neurobiol 7:599–604. https://doi.org/10.1016/S0959-4388(97)80078-5
Hong J, Zhang H, Kawase-Koga Y, Sun T (2013) MicroRNA function is required for neurite outgrowth of mature neurons in the mouse postnatal cerebral cortex. Front Cell Neurosci 7:151. https://doi.org/10.3389/fncel.2013.00151
Horbinski C, Stachowiak MK, Higgins D, Finnegan SG (2001) Polyethyleneimine-mediated transfection of cultured postmitotic neurons from rat sympathetic ganglia and adult human retina. BMC Neurosci 2:2. https://doi.org/10.1186/1471-2202-2-2
Impey S, Davare M, Lasiek A et al (2010) An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling. Mol Cell Neurosci 43:146–156
Irie K, Tsujimura K, Nakashima H, Nakashima K (2016) MicroRNA-214 promotes dendritic development by targeting the Schizophrenia-associated gene Quaking (Qki). J Biol Chem 291:13891–13904. https://doi.org/10.1074/jbc.M115.705749
Ishteiwy RA, Ward TM, Dykxhoorn DM, Burnstein KL (2012) The microRNA -23b/-27b cluster suppresses the metastatic phenotype of castration-resistant prostate cancer cells. PLoS ONE 7:e52106. https://doi.org/10.1371/journal.pone.0052106
Jackson KL, Marques FZ, Watson AMD et al (2013) A novel interaction between sympathetic overactivity and aberrant regulation of renin by miR-181a in BPH/2 J genetically hypertensive mice. Hypertension 62:775–781. https://doi.org/10.1161/HYPERTENSIONAHA.113.01701
Kang H, Davis-Dusenbery BN, Nguyen PH et al (2012) Bone morphogenetic protein 4 promotes vascular smooth muscle contractility by activating microRNA-21 (miR-21), which down-regulates expression of family of dedicator of cytokinesis (DOCK) proteins. J Biol Chem 287:3976–3986. https://doi.org/10.1074/jbc.M111.303156
Katchy A, Williams C (2014) Profiling of estrogen-regulated microRNAs in breast cancer cells. J Vis Exp. https://doi.org/10.3791/51285
Kaufmann WE, Moser HW (2000) Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 10:981–991
Kim I-J, Beck HN, Lein PJ, Higgins D (2002) Interferon gamma induces retrograde dendritic retraction and inhibits synapse formation. J Neurosci 22:4530–4539
Kim I-J, Drahushuk KM, Kim W-Y et al (2004) Extracellular signal-regulated kinases regulate dendritic growth in rat sympathetic neurons. J Neurosci 24:3304–3312. https://doi.org/10.1523/JNEUROSCI.3286-03.2004
Kim W-Y, Gonsiorek EA, Barnhart C et al (2009) Statins decrease dendritic arborization in rat sympathetic neurons by blocking RhoA activation. J Neurochem 108:1057–1071
Kishi T, Hirooka Y, Mukai Y et al (2003) Atorvastatin causes depressor and sympatho-inhibitory effects with upregulation of nitric oxide synthases in stroke-prone spontaneously hypertensive rats. J Hypertens 21:379–386. https://doi.org/10.1097/01.hjh.0000052443.12292.22
Kondo M, Terada M, Shimizu D et al (1990) Morphometric study of the superior cervical and stellate ganglia of spontaneously hypertensive rats during the prehypertensive stage. Virchows Arch B Cell Pathol Incl Mol Pathol 58:371–376
Konopka W, Schütz G, Kaczmarek L (2011) The microRNA contribution to learning and memory. Neuroscientist 17:468–474
Kosik KS (2006) The neuronal microRNA system. Nat Rev Neurosci 7:911–920
Kulkarni VA, Firestein BL (2012) The dendritic tree and brain disorders. Mol Cell Neurosci 50:10–20. https://doi.org/10.1016/J.MCN.2012.03.005
Kye MJ, Neveu P, Lee Y-S et al (2011) NMDA mediated contextual conditioning changes miRNA expression. PLoS ONE 6:e24682. https://doi.org/10.1371/journal.pone.0024682
Leggio L, Vivarelli S, L’Episcopo F et al (2017) microRNAs in Parkinson’s disease: from pathogenesis to novel diagnostic and therapeutic approaches. Int J Mol Sci 1:2. https://doi.org/10.3390/ijms18122698
Lein P, Johnson M, Guo X et al (1995) Osteogenic protein-1 induces dendritic growth in rat sympathetic neurons. Neuron 15:597–605
Lein PJ, Guo X, Shi GX et al (2007) The novel GTPase Rit differentially regulates axonal and dendritic growth. J Neurosci 27:4725–4736
Lein PJ, Fryer A, Higgins D (2010) Cell culture: autonomic and enteric neurons. In: Squire LR (ed) Encyclopedia of Neuroscience. Elsevier Ltd, California, pp 625–632
Li B, Sun H (2013) miR-26a promotes neurite outgrowth by repressing PTEN expression. Mol Med Rep 8:676–680. https://doi.org/10.3892/mmr.2013.1534
Li X, Wei Y, Wang Z (2018) microRNA-21 and hypertension. Hypertens Res 41:649–661. https://doi.org/10.1038/s41440-018-0071-z
Liu FJ, Kaur P, Karolina DS et al (2015) MiR-335 regulates Hif-1α to reduce cell death in both mouse cell line and rat ischemic models. PLoS ONE 10:e0128432. https://doi.org/10.1371/journal.pone.0128432
Liu H, Hao W, Wang X, Su H (2016) miR-23b targets Smad 3 and ameliorates the LPS-inhibited osteogenic differentiation in preosteoblast MC3T3-E1 cells. J Toxicol Sci 41:185–193. https://doi.org/10.2131/jts.41.185
Luzi E, Marini F, Sala SC et al (2008) Osteogenic differentiation of human adipose tissue-derived stem cells is modulated by the miR-26a targeting of the SMAD1 transcription factor. J Bone Miner Res 23:287–295. https://doi.org/10.1359/jbmr.071011
Maciotta S, Meregalli M, Torrente Y (2013) The involvement of microRNAs in neurodegenerative diseases. Front Cell Neurosci 7:265. https://doi.org/10.3389/fncel.2013.00265
Magill ST, Cambronne XA, Luikart BW et al (2010) microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc Natl Acad Sci USA 107:20382–20387
Merola A, Romagnolo A, Rosso M et al (2018) Autonomic dysfunction in Parkinson’s disease: a prospective cohort study. Mov Disord 33:391–397. https://doi.org/10.1002/mds.27268
Mestdagh P, Hartmann N, Baeriswyl L et al (2014) Evaluation of quantitative miRNA expression platforms in the microRNA quality control (miRQC) study. Nat Methods 11:809–815. https://doi.org/10.1038/nmeth.3014
Meza-Sosa KF, Pedraza-Alva G, Perez-Martinez L (2014) microRNAs: key triggers of neuronal cell fate. Front Cell Neurosci 8:175. https://doi.org/10.3389/fncel.2014.00175
Natera-Naranjo O, Aschrafi A, Gioio AE, Kaplan BB (2010) Identification and quantitative analyses of microRNAs located in the distal axons of sympathetic neurons. RNA 16:1516–1529
Norcini M, Sideris A, Martin Hernandez LA et al (2014) An approach to identify microRNAs involved in neuropathic pain following a peripheral nerve injury. Front Neurosci 8:266. https://doi.org/10.3389/fnins.2014.00266
Pardo CA, Eberhart CG (2007) The neurobiology of Autism. Brain Pathol 17:434–447. https://doi.org/10.1111/j.1750-3639.2007.00102.x
Pavlopoulos E, Trifilieff P, Chevaleyre V et al (2011) Neuralized1 activates CPEB3: a function for nonproteolytic ubiquitin in synaptic plasticity and memory storage. Cell 147:1369–1383. https://doi.org/10.1016/j.cell.2011.09.056
Penzes P, Cahill ME, Jones KA et al (2011) Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 14:285–293. https://doi.org/10.1038/nn.2741
Peruzzi D, Hendley ED, Forehand CJ (1991) Hypertrophy of stellate ganglion cells in hypertensive, but not hyperactive, rats. Am J Physiol 261:R979–R984. https://doi.org/10.1152/ajpregu.1991.261.4.R979
Purves D (1975) Functional and structural changes in mammalian sympathetic neurones following interruption of their axons. J Physiol 252:429–463
Purves D, Hume RI (1981) The relation of postsynaptic geometry to the number of presynaptic axons that innervate autonomic ganglION. J Neurosci 1:441–452
Purves D, Lichtman JW (1985) Geometrical differences among homologous neurons in mammals. Science 228:298–302
Purves D, Hadley RD, Voyvodic JT (1986) Dynamic changes in the dendritic geometry of individual neurons visualized over periods of up to three months in the superior cervical ganglion of living mice. J Neurosci 6:1051–1060. https://doi.org/10.1523/JNEUROSCI.06-04-01051.1986
Qin W, Zhao B, Shi Y et al (2009) BMPRII is a direct target of miR-21. Acta Biochim Biophys Sin (Shanghai) 41:618–623
Reales E, Bernabé-Rubio M, Casares-Arias J et al (2015) The MAL protein is crucial for proper membrane condensation at the ciliary base, which is required for primary cilium elongation. J Cell Sci 128:2261–2270. https://doi.org/10.1242/jcs.164970
Reinke C, Carthew R (2008) BMP signaling goes posttranscriptional in a microRNA sort of way. Dev Cell 15:174–175
Rogler CE, LeVoci L, Ader T et al (2009) MicroRNA-23b cluster microRNAs regulate transforming growth factor-beta/bone morphogenetic protein signaling and liver stem cell differentiation by targeting Smads. Hepatology 50:575–584. https://doi.org/10.1002/hep.22982
Rubin E (1985) Development of the rat superior cervical ganglion: initial stages of synapse formation. J Neurosci 5:697–704
Saj A, Lai EC (2011) Control of microRNA biogenesis and transcription by cell signaling pathways. Curr Opin Genet Dev 21:504–510
Sandoval-Bórquez A, Polakovicova I, Carrasco-Véliz N et al (2017) MicroRNA-335-5p is a potential suppressor of metastasis and invasion in gastric cancer. Clin Epigenetics 9:114. https://doi.org/10.1186/s13148-017-0413-8
Sathyan P, Golden HB, Miranda RC (2007) Competing interactions between micro-RNAs determine neural progenitor survival and proliferation after ethanol exposure: evidence from an ex vivo model of the fetal cerebral cortical neuroepithelium. J Neurosci 27:8546–8557. https://doi.org/10.1523/JNEUROSCI.1269-07.2007
Shi L, Liao J, Liu B et al (2015) Mechanisms and therapeutic potential of microRNAs in hypertension. Drug Discov Today 20:1188–1204. https://doi.org/10.1016/j.drudis.2015.05.007
Shinde S, Mukhopadhyay S, Mohsen G, Khoo SK (2015) Biofluid-based microRNA biomarkers for Parkinson’s disease: an overview and update. Peer Rev Artic 2:15–25
Siegel G, Obernosterer G, Fiore R et al (2009) A functional screen implicates microRNA-138- dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat Cell Biol 11:705. https://doi.org/10.1038/ncb1876
Smolen AJ, Wright LL, Cunningham TJ (1983) Neuron numbers in the superior cervical sympathetic ganglion of the rat: a critical comparison of methods for cell counting. J Neurocytol 12:739–750. https://doi.org/10.1007/BF01258148
Strickland IT, Richards L, Holmes FE et al (2011) Axotomy-induced miR-21 promotes axon growth in adult dorsal root ganglion neurons. PLoS ONE 6:e23423
Su X, Liao L, Shuai Y et al (2015) MiR-26a functions oppositely in osteogenic differentiation of BMSCs and ADSCs depending on distinct activation and roles of Wnt and BMP signaling pathway. Cell Death Dis 6:e1851–e1851. https://doi.org/10.1038/cddis.2015.221
Supekar K, Uddin LQ, Khouzam A et al (2013) Brain hyperconnectivity in children with autism and its links to social deficits. Cell Rep 5:738–747. https://doi.org/10.1016/j.celrep.2013.10.001
Tai H-C, Schuman EM (2006) MicroRNA: microRNAs Reach out into Dendrites. Curr Biol 16:R121–R123. https://doi.org/10.1016/J.CUB.2006.02.006
van Spronsen M, van Battum EY, Kuijpers M et al (2013) Developmental and activity-dependent miRNA expression profiling in primary hippocampal neuron cultures. PLoS ONE 8:e74907. https://doi.org/10.1371/journal.pone.0074907
Vigelsø A, Dybboe R, Hansen CN et al (2015) GAPDH and β-actin protein decreases with aging, making Stain-Free technology a superior loading control in Western blotting of human skeletal muscle. J Appl Physiol 118:386–394. https://doi.org/10.1152/japplphysiol.00840.2014
Wang J, Greene SB, Bonilla-Claudio M et al (2010) Bmp signaling regulates myocardial differentiation from cardiac progenitors through a MicroRNA-mediated mechanism. Dev Cell 19:903–912
Wei C, Henderson H, Spradley C et al (2013) Circulating miRNAs as potential marker for pulmonary hypertension. PLoS ONE 8:e64396. https://doi.org/10.1371/journal.pone.0064396
Wotton D, Massague J (2000) Transcriptional control by the TGF- b/Smad signaling system. EMBO J 19:1745–1754
Wu T, Chen W, Liu S et al (2014) Huaier suppresses proliferation and induces apoptosis in human pulmonary cancer cells via upregulation of miR-26b-5p. FEBS Lett 588:2107–2114. https://doi.org/10.1016/j.febslet.2014.04.044
Yuan M, Tang Y, Zhou C et al (2016) Elevated plasma CaM expression in patients with acute cerebral infarction predicts poor outcomes and is inversely associated with miR-26b expression. Int J Neurosci 126:408–414. https://doi.org/10.3109/00207454.2015.1020537
Zhou X et al (2012) MicroRNA Profiling Using µParaflo Microfluidic Array Technology. In: Fan JB (ed) Next-generation MicroRNA expression profiling technology. Humana Press, New York, pp 153–182
Acknowledgements
We thank Donald Bruun and Hao Chen at UC Davis for assistance in setting up and maintaining sympathetic cultures.
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This work was supported by the Saint Mary’s College Summer Research Program (KP, ST, TB) Faculty Development Fund (VC), Faculty Research Grant (VC), and by the National Institute of Environmental Health Sciences (grants ES014901 and ES017592 to PJL). The funding agencies were not involved in the study design, in the collection, analysis, or interpretation of data, in the writing of the report, or in the decision to submit the paper for publication.
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KP did most of the qpCR analysis and the functional studies on individual miRNAs, and helped draft the manuscript. KW completed the functional studies, ST did the microarray studies, and TB and KT helped with the optimization of the qPCR analysis and the functional studies using GAPDH siRNA. PL provided the funding and resources for animal work, and VC designed the study, provided some of the funding for the study, isolated neurons for the study, supervised the students during experimental setup and data analysis, and wrote the manuscript.
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of University of California at Davis and Saint Mary’s College of California, where these studies were conducted. This article does not contain any studies with human participants performed by any of the authors.
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Pravoverov, K., Whiting, K., Thapa, S. et al. MicroRNAs are Necessary for BMP-7-induced Dendritic Growth in Cultured Rat Sympathetic Neurons. Cell Mol Neurobiol 39, 917–934 (2019). https://doi.org/10.1007/s10571-019-00688-2
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DOI: https://doi.org/10.1007/s10571-019-00688-2