Skeletal Muscle's Role in Prenatal Inter-organ Communication: A Phenogenomic Study with Qualitative Citation Analysis.
Cell interactions
Embryonic development
Skeletal muscle
Tissue interactions
Journal
Advances in anatomy, embryology, and cell biology
ISSN: 0301-5556
Titre abrégé: Adv Anat Embryol Cell Biol
Pays: Germany
ID NLM: 0407712
Informations de publication
Date de publication:
2023
2023
Historique:
medline:
14
11
2023
pubmed:
13
11
2023
entrez:
13
11
2023
Statut:
ppublish
Résumé
Gene targeting in mice allows for a complete elimination of skeletal (striated or voluntary) musculature in the body, from the beginning of its development, resulting in our ability to study the consequences of this ablation on other organs. Here I focus on the relationship between the muscle and lung, motor neurons, skeleton, and special senses. Since the inception of my independent laboratory, in 2000, with my team, we published more than 30 papers (and a book chapter), nearly 400 pages of data, on these specific relationships. Here I trace, using Web of Science, nearly 600 citations of this work, to understand its impact. The current report contains a summary of our work and its impact, NCBI's Gene Expression Omnibus accession numbers of all our microarray data, and three clear future directions doable by anyone using our publicly available data. Together, this effort furthers our understanding of inter-organ communication during prenatal development.
Identifiants
pubmed: 37955769
doi: 10.1007/978-3-031-38215-4_1
doi:
Substances chimiques
Vitamins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1-19Informations de copyright
© 2023. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Angka HE, Kablar B (2007) Differential responses to the application of exogenous NT-3 are observed for subpopulations of motor and sensory neurons depending on the presence of skeletal muscle. Dev Dyn 236:1193–1202
pubmed: 17436272
doi: 10.1002/dvdy.21147
Angka HE, Kablar B (2009) Role of skeletal muscle in the epigenetic shaping of motor neuron fate choices. Histol Histopathol 24:1579–1592
pubmed: 19795356
Angka HE, Geddes AJ, Kablar B (2008) Differential survival response of neurons to exogenous GDNF depends on the presence of skeletal muscle. Dev Dyn 237:3169–3178
pubmed: 18816441
doi: 10.1002/dvdy.21727
Baguma-Nibasheka M, Kablar B (2008) Pulmonary hypoplasia in the connective tissue growth factor (Ctgf) null mouse. Dev Dyn 237:485–493
pubmed: 18213577
doi: 10.1002/dvdy.21433
Baguma-Nibasheka M, Kablar B (2009a) Abnormal retinal development in the Btrc null mouse. Dev Dyn 238:2680–2687
pubmed: 19705444
pmcid: 5021536
doi: 10.1002/dvdy.22081
Baguma-Nibasheka M, Kablar B (2009b) Altered retinal cell differentiation in the AP-3 delta mutant (Mocha) mouse. Int J Dev Neurosci 27:701–708
pubmed: 19631730
doi: 10.1016/j.ijdevneu.2009.07.005
Baguma-Nibasheka M, Reddy T, Abbas-Butt A et al (2006) Fetal ocular movements and retinal cell differentiation: analysis employing DNA microarrays. Histol Histopathol 21:1331–1337
pubmed: 16977584
Baguma-Nibasheka M, Angka HE, Inanlou MR et al (2007) Microarray analysis of Myf5−/−:MyoD−/− hypoplastic mouse lungs reveals a profile of genes involved in pneumocyte differentiation. Histol Histopathol 22:483–495
pubmed: 17330803
Baguma-Nibasheka M, Gugic D, Saraga-Babic M et al (2012) Role of skeletal muscle in lung development. Histol Histopathol 27:817–826
Baguma-Nibasheka M, Fracassi A, Costain WJ et al (2016) Role of skeletal muscle in motor neuron development. Histol Histopathol 31:699–719
pubmed: 26892388
Baguma-Nibasheka M, Fracassi A, Costain WJ et al (2019) Striated-for-smooth muscle replacement in the developing mouse esophagus. Histol Histopathol 34:457–467
pubmed: 30698269
Barlow JP, Solomon TP (2018) Do skeletal muscle-secreted factors influence the function of pancreatic β-cells? Am J Physiol Endocrinol Metab 314:E297–E307
pubmed: 29208613
doi: 10.1152/ajpendo.00353.2017
Bytyqi AH, Lockridge O, Duysen E et al (2004) Impaired formation of the inner retina in an AChE knockout mouse results in degeneration of all photoreceptors. Eur J Neurosci 20:2953–2962
pubmed: 15579149
doi: 10.1111/j.1460-9568.2004.03753.x
Calle EA, Ghaedi M, Sundaram S et al (2014) Strategies for whole lung tissue engineering. IEEE Trans Biomed Eng 61:1482–1496
pubmed: 24691527
pmcid: 4126648
doi: 10.1109/TBME.2014.2314261
Chal J, Al Tanoury Z, Oginuma M et al (2018) Recapitulating early development of mouse musculoskeletal precursors of the paraxial mesoderm in vitro. Development. https://doi.org/10.1242/dev.157339
Chan CJ, Costanzo M, Ruiz-Herrero T et al (2019) Hydraulic control of mammalian embryo size and cell fate. Nature 571:112–116
pubmed: 31189957
doi: 10.1038/s41586-019-1309-x
Chen Q, Zhao Y, Qian Y et al (2019) A genetic-phenotypic classification for syndromic micrognathia. J Hum Genet 64:875–883
pubmed: 31273320
doi: 10.1038/s10038-019-0630-4
Chen T, Liu Z, Xue C et al (2020) Association of dysplastic coronoid process with long-face morphology. J Dent Res 99:339–348
pubmed: 31826728
doi: 10.1177/0022034519892551
Cheng CP, Liu YC, Tsai YL et al (2013) An efficient method for mining cross-timepoint gene regulation sequential patterns from time course gene expression datasets. BMC Bioinform. https://doi.org/10.1186/1471-2105-14-S12-S3
Cohen JC, Larson JE (2008) The Peter Pan paradigm. Theor Biol Med Model. https://doi.org/10.1186/1742-4682-5-1
Comai G, Sambasivan R, Gopalakrishnan S et al (2014) Variations in the efficiency of lineage marking and ablation confound distinctions between myogenic cell populations. Dev Cell 31:654–667
pubmed: 25490270
doi: 10.1016/j.devcel.2014.11.005
De Vries JIP, Fong BF (2007) Changes in fetal motility as a result of congenital disorders: an overview. Ultrasound Obstet Gynecol 29:590–599
pubmed: 17427894
doi: 10.1002/uog.3917
Dijkstra AE, Smolonska J, van den Berge M et al (2014) Susceptibility to chronic mucus hypersecretion, a genome wide association study. PLoS One. https://doi.org/10.1371/journal.pone.0091621
Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207–210
pubmed: 11752295
pmcid: 99122
doi: 10.1093/nar/30.1.207
Fauroux B, Lofaso F (2005) Non-invasive mechanical ventilation: when to start for what benefit? Thorax 60:979–980
pubmed: 16299111
pmcid: 1747262
doi: 10.1136/thx.2005.040394
Feingold-Zadok M, Chitayat D, Chong K et al (2017) Mutations in the NEB gene cause fetal akinesia/arthrogryposis multiplex congenital. Prenat Diagn 37:144–150
pubmed: 27933661
doi: 10.1002/pd.4977
Felsenthal N, Zelzer E (2017) Mechanical regulation of musculoskeletal system development. Development 144:4271–4283
pubmed: 29183940
pmcid: 6514418
doi: 10.1242/dev.151266
Filges I, Hall JG (2013) Failure to identify antenatal multiple congenital contractures and fetal akinesia--proposal of guidelines to improve diagnosis. Prenat Diagn 33:61–74
Geddes AJ, Angka HE, Davies KA et al (2006) Subpopulations of motor and sensory neurons respond differently to brain-derived neurotrophic factor depending on the presence of the skeletal muscle. Dev Dyn 235:2175–2184
pubmed: 16804896
doi: 10.1002/dvdy.20877
Gerhart J, Pfautz J, Neely C et al (2009) Noggin producing, MyoD-positive cells are crucial for eye development. Dev Biol 336:30–41
pubmed: 19778533
pmcid: 2783511
doi: 10.1016/j.ydbio.2009.09.022
Glatzel-Plucinska N, Piotrowska A, Grzegrzolka J et al (2018) SATB1 level correlates with Ki-67 expression and is a positive prognostic factor in non-small cell lung carcinoma. Anticancer Res 38:723–736
pubmed: 29374696
Gomez C, David V, Peet NM et al (2007) Absence of mechanical loading in utero influences bone mass and architecture but not innervation in Myod-Myf5-deficient mice. J Anat 210:259–271
pubmed: 17331176
pmcid: 2100282
doi: 10.1111/j.1469-7580.2007.00698.x
Hall-Glenn F, Lyons KM (2011) Roles for CCN2 in normal physiological processes. Cell Mol Life Sci 68:3209–3217
pubmed: 21858450
pmcid: 3670951
doi: 10.1007/s00018-011-0782-7
Hernandez-Hernandez JM, Garcia-Gonzalez EG, Brun CE et al (2017) The myogenic regulatory factors, determinants of muscle development, cell identity and regeneration. Semin Cell Dev Biol 72:10–18
pubmed: 29127045
pmcid: 5723221
doi: 10.1016/j.semcdb.2017.11.010
Hill DP, Berardini TZ, Howe DG et al (2010) Representing ontogeny through ontology: a developmental biologist’s guide to the gene ontology. Mol Reprod Dev 77:314–329
pubmed: 19921742
pmcid: 2830379
doi: 10.1002/mrd.21130
Holbourn KP, Acharya KR, Perbal B (2008) The CCN family of proteins: structure-function relationships. Trends Biochem Sci 33:461–473
pubmed: 18789696
pmcid: 2683937
doi: 10.1016/j.tibs.2008.07.006
Hollo G (2017) Demystification of animal symmetry: symmetry is a response to mechanical forces. Biol Direct. https://doi.org/10.1186/s13062-017-0182-5
Hong P, Rot I, Kablar B (2015) The role of skeletal muscle in external ear development: a mouse model histomorphometric study. Plast Reconstr Surg Glob Open. https://doi.org/10.1097/GOX.0000000000000352
Iizuka K, Machida T, Hirafuji M (2014) Skeletal muscle is an endocrine organ. J Pharmacol Sci 125:125–131
pubmed: 24859778
doi: 10.1254/jphs.14R02CP
Inanlou MR, Kablar B (2003) Abnormal development of the diaphragm in mdx:MyoD−/− 9th embryos leads to pulmonary hypoplasia. Int J Dev Biol 47:363–371
pubmed: 12895031
Inanlou MR, Kablar B (2005) Contractile activity of skeletal musculature involved in breathing is essential for normal lung cell differentiation, as revealed in Myf5−/−:MyoD−/− embryos. Dev Dyn 233:772–782
pubmed: 15844178
doi: 10.1002/dvdy.20381
Inanlou MR, Baguma-Nibasheka M, Kablar B (2005) The role of fetal breathing-like movements in lung organogenesis. Histol Histopathol 20:1261–1266
pubmed: 16136506
Jun JI, Lau LF (2011) Taking aim at the extracellular matrix: CCN proteins as emerging therapeutic targets. Nat Rev Drug Discov 10:945–963
pubmed: 22129992
pmcid: 3663145
doi: 10.1038/nrd3599
Kablar B (2003) Determination of retinal cell fates is affected in the absence of extraocular striated muscles. Dev Dyn 226:478–490
pubmed: 12619134
doi: 10.1002/dvdy.10256
Kablar B (2011) Role of skeletal musculature in the epigenetic shaping of organs, tissues and cell fate choices. In: Hallgrimsson B, Hall BK (eds) Epigenetics, linking genotype and phenotype in development and evolution, 1st edn. University of California Press, Berkely, LA, pp 256–268
Kablar B, Belliveau AC (2005) Presence of neurotrophic factors in skeletal muscle correlates with survival of spinal cord motor neurons. Dev Dyn 234:659–669
pubmed: 16193506
doi: 10.1002/dvdy.20589
Kablar B, Rudnicki MA (1999) Development in the absence of skeletal muscle results in the sequential ablation of motor neurons from the spinal cord to the brain. Dev Biol 208:93–109
pubmed: 10075844
doi: 10.1006/dbio.1998.9184
Karsenty G, Olson EN (2016) Bone and muscle endocrine functions: unexpected paradigms of inter-organ communication. Cell 164:1248–1256
pubmed: 26967290
pmcid: 4797632
doi: 10.1016/j.cell.2016.02.043
Karstoft K, Pedersen BK (2016) Skeletal muscle as a gene regulatory endocrine organ. Curr Opin Clin Nutr Metab Care 19:270–275
pubmed: 27101470
doi: 10.1097/MCO.0000000000000283
Kassar-Duchossoy L, Gayraud-Morel B, Gomes D et al (2004) Mrf4 determines skeletal muscle identity in Myf5:MyoD double-mutant mice. Nature 431:466–471
pubmed: 15386014
doi: 10.1038/nature02876
Kato S, Yokoyama S, Hayakawa Y et al (2016) P38 pathway as a key downstream signal of connective tissue growth factor to regulate metastatic potential in non-small-cell lung cancer. Cancer Sci 107:1416–1421
pubmed: 27403934
pmcid: 5084657
doi: 10.1111/cas.13009
Knausgaard KO (2012) My struggle. Random House, London
Kouskoura T, El Fersioui Y, Angelini M et al (2016) Dislocated tongue muscle attachment connected to cleft palate formation. J Dent Res 95:453–459
pubmed: 26701347
doi: 10.1177/0022034515621869
Kozhemyakina E, Lassar AB, Zelzer E (2015) A pathway to bone: signaling molecules and transcription factors involved in chondrocyte development and maturation. Development 142:817–831
pubmed: 25715393
pmcid: 4352987
doi: 10.1242/dev.105536
Kuznetsov MS, Rezvyakov PN, Lisyukov AN et al (2019a) Bioinformatic analysis of the sciatic nerve transcriptomes of mice after 30-Day spaceflight on board the Bion-M1 biosatellite. Russ J Genet 55:388–392
doi: 10.1134/S1022795419030104
Kuznetsov MS, Lisukov AN, Rizvanov AA et al (2019b) Bioinformatic study of transcriptome changes in the mice lumbar spinal cord after the 30-day spaceflight and subsequent 7-day readaptation on earth: new insights into molecular mechanisms of the hypogravity motor syndrome. Front Pharmacol. https://doi.org/10.3389/fphar.2019.00747
Lecuit T, Mahadevan L (2017) Morphogenesis one century after On Growth and Form. Development 144:4197–4198
pubmed: 29183932
doi: 10.1242/dev.161125
Li J, Ye L, Owen S et al (2015) Emerging role of CCN family proteins in tumorigenesis and cancer metastasis. Int J Mol Med 36:1451–1463
pubmed: 26498181
pmcid: 4678164
doi: 10.3892/ijmm.2015.2390
Li J, Wang Z, Chu Q et al (2018) The strength of mechanical forces determines the differentiation of alveolar epithelial cells. Dev Cell 44:297–312
pubmed: 29408236
doi: 10.1016/j.devcel.2018.01.008
Longo G, Montevil M, Sonnenschein C et al (2015) In search of principles for a theory of organisms. J Biosci. https://doi.org/10.1007/s12038-015-9574-9
Mammoto T, Ingber DE (2010) Mechanical control of tissue and organ development. Development 137:1407–1420
pubmed: 20388652
pmcid: 2853843
doi: 10.1242/dev.024166
Mammoto T, Mammoto A, Ingber DE (2013) Mechanobiology and developmental control. Annu Rev Cell Dev Biol 29:27–61
pubmed: 24099083
doi: 10.1146/annurev-cellbio-101512-122340
Maurel DB, Jahn K, Lara-Castillo N (2017) Muscle-bone crosstalk: emerging opportunities for novel therapeutic approaches to treat musculoskeletal pathologies. Biomedicine. https://doi.org/10.3390/biomedicines5040062
Mescher AL (2016) Junqueira’s Basic Histology Text and Atlas. McGraw Hill Education, New York
Moreno E, Rhiner C (2014) Darwin's multicellularity: from neurotrophic theories and cell competition to fitness fingerprints. Curr Opin Cell Biol 31:16–22
pubmed: 25022356
pmcid: 4238900
doi: 10.1016/j.ceb.2014.06.011
Moss ML (1997) The functional matrix hypothesis revisited. 1. The role of mechanotransduction. Am J Orthod Dentofac Orthop 112:8–11
doi: 10.1016/S0889-5406(97)70267-1
Mukhopadhyay P, Seelan RS, Rezzoug F et al (2017) Determinants of orofacial clefting I: effects of 5-aza-2′-deoxycytidine on cellular processes and gene expression during development of the first branchial arch. Reprod Toxicol 67:85–99
pubmed: 27915011
doi: 10.1016/j.reprotox.2016.11.016
Müller GB, Newman SA (2003) Origination of organismal form: beyond the gene in developmental and evolutionary biology. MIT Press, Cambridge
doi: 10.7551/mitpress/5182.001.0001
Nayak MS, Kim YS, Goldman M et al (2006) Cellular therapies in motor neuron diseases. Biochim Biophys Acta 1762:1128–1138
pubmed: 16872810
doi: 10.1016/j.bbadis.2006.06.004
Nelson CM, Gleghorn JP, Pang MF et al (2017) Microfluidic chest cavities reveal that transmural pressure controls the rate of lung development. Development 144:4328–4335
pubmed: 29084801
pmcid: 5769635
Noden DM, Francis-West P (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:1194–1218
pubmed: 16502415
doi: 10.1002/dvdy.20697
Nowlan NC (2015) Biomechanics of foetal movement. Eur Cell Mater 29:1–21
pubmed: 25552425
doi: 10.22203/eCM.v029a01
Nowlan NC, Dumas G, Tajbakhsh S et al (2012) Biophysical stimuli induced by passive movements compensate for lack of skeletal muscle during embryonic skeletogenesis. Biomech Model Mechanobiol 11:207–219
pubmed: 21505895
doi: 10.1007/s10237-011-0304-4
Ornitz DM, Yin Y (2012) Signaling networks regulating development of the lower respiratory tract. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a008318
Petersen TH, Calle EA, Niklason LE (2011) Strategies for lung regeneration. Mater Today 14:196–201
doi: 10.1016/S1369-7021(11)70114-6
Petersen TH, Calle EA, Colehour MB et al (2012) Matrix composition and mechanics of decellularized lung scaffolds. Cells Tissues Organs 195:222–231
pubmed: 21502745
doi: 10.1159/000324896
Piccolo S (2013) Developmental biology: Mechanics in the embryo. Nature 504:223–225
pubmed: 24336279
doi: 10.1038/504223a
Pollard AS, Boyd S, McGonnell IM et al (2017) The role of embryo movement in the development of the furcula. J Anat 230:435–443
pubmed: 27921302
doi: 10.1111/joa.12571
Rolfe R, Roddy K, Murphy P (2013) Mechanical regulation of skeletal development. Curr Osteoporos Rep 11:107–116
pubmed: 23467901
doi: 10.1007/s11914-013-0137-4
Rot I, Kablar B (2010) The influence of acoustic and static stimuli on development of inner ear sensory epithelia. Int J Dev Neurosci 28:309–315
pubmed: 20188812
doi: 10.1016/j.ijdevneu.2010.02.008
Rot I, Kablar B (2013) Role of skeletal muscle in palate development. Histol Histopathol 28:1–13
pubmed: 23233055
Rot I, Mardesic-Brakus S, Costain WJ et al (2014) Role of skeletal muscle in mandible development. Histol Histopathol 29:1377–1394
pubmed: 24867377
Rot I, Baguma-Nibasheka M, Costain WJ et al (2017) Role of skeletal muscle in ear development. Histol Histopathol 32:987–1000
pubmed: 28271491
Rot-Nikcevic I, Reddy T, Downing KJ et al (2006) Myf5
pubmed: 16208536
doi: 10.1007/s00427-005-0024-9
Rot-Nikcevic I, Downing KJ, Hall BK et al (2007) Development of the mouse mandibles and clavicles in the absence of skeletal myogenesis. Histol Histopathol 22:51–60
pubmed: 17128411
Rudnicki MA, Schnegelsberg PN, Stead RH et al (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75:1351–1359
pubmed: 8269513
doi: 10.1016/0092-8674(93)90621-V
Sadler TW (2012) Langman’s medical embryology. Lippincott Williams & Wilkins, Philadelphia
Sarnat HB (1994) New insights into the pathogenesis of congenital myopathies. J Child Neurol 9:193–201
pubmed: 8006374
doi: 10.1177/088307389400900218
Selinger CI, Cooper WA, Al-Sohaily S et al (2011) Loss of special AT-rich binding protein 1 expression is a marker of poor survival in lung cancer. J Thorac Oncol 6:1179–1189
pubmed: 21597389
doi: 10.1097/JTO.0b013e31821b4ce0
Severinsen MCK, Pedersen BK (2020) Muscle-organ crosstalk: the emerging roles of myokines. Endocr Rev 41:594–609
pubmed: 32393961
pmcid: 7288608
doi: 10.1210/endrev/bnaa016
Shea CA, Rolfe RA, Murphy P (2015) The importance of foetal movement for co-ordinated cartilage and bone development in utero. Bone Joint Res 4:105–116
pubmed: 26142413
pmcid: 4602203
doi: 10.1302/2046-3758.47.2000387
Simonds AK (2006) Recent advances in respiratory care for neuromuscular disease. Chest 130:1879–1886
pubmed: 17167012
doi: 10.1378/chest.130.6.1879
Smith CM, Finger JH, Kadin JA et al (2014) Gene Expression Database for mouse development (GXD): putting developmental expression information at your fingertips. Dev Dyn 243:1176–1186
pubmed: 24958384
pmcid: 4415381
doi: 10.1002/dvdy.24155
Sugimura K, Lenne PF, Graner F (2016) Measuring forces and stresses in situ in living tissues. Development 143:186–196
pubmed: 26786209
doi: 10.1242/dev.119776
Suzuki M, Svendsen CN (2008) Combining growth factor and stem cell therapy for amyotrophic lateral sclerosis. Trends Neurosci 31:192–198
pubmed: 18329734
doi: 10.1016/j.tins.2008.01.006
Thompson DW (1917) On Growth and Form. Cambridge University Press, Cambridge
doi: 10.5962/bhl.title.11332
Tovar-y-Romo LB, Ramirez-Jarquin UN, Lazo-Gomez R et al (2014) Trophic factors as modulators of motor neuron physiology and survival: implications for ALS therapy. Front Cell Neurosci. https://doi.org/10.3389/fncel.2014.00061
Urbanska M, Winzi M, Neumann K et al (2017) Single-cell mechanical phenotype is an intrinsic marker of reprogramming and differentiation along the mouse neural lineage. Development 144:4313–4321
pubmed: 29183942
doi: 10.1242/dev.155218
Warburton D, El-Hashash A, Carraro G et al (2010) Lung organogenesis. Curr Top Dev Biol 90:73–158
pubmed: 20691848
pmcid: 3340128
doi: 10.1016/S0070-2153(10)90003-3
Woronowicz KC, Schneider RA (2019) Molecular and cellular mechanisms underlying the evolution of form and function in the amniote jaw. EvoDevo. https://doi.org/10.1186/s13227-019-0131-8
Wulf A (2015) The invention of nature: Alexander von Humboldt’s new world. Alfred A. Knopf, New York
Xu HY, Xue JX, Gao H et al (2019) Fluvastatin-mediated down-regulation of SATB1 affects aggressive phenotypes of human non-small-cell lung cancer cell line H292. Life Sci 222:212–220
pubmed: 30557545
doi: 10.1016/j.lfs.2018.12.022
Zelditch ML, Wood AR, Bonett RM et al (2008) Modularity of the rodent mandible: Integrating bones, muscles, and teeth. Evol Dev 10:756–768
pubmed: 19021747
doi: 10.1111/j.1525-142X.2008.00290.x
Zhang J, Yang Z, Wu SM (2005) Development of cholinergic amacrine cells is visual activity-dependent in the postnatal mouse retina. J Comp Neurol 484:331–343
pubmed: 15739235
doi: 10.1002/cne.20470
Zhang J, Wu D, Turnbull DH (2018) In utero MRI of mouse embryos. Methods Mol Biol 1718:285–296
pubmed: 29341015
pmcid: 6091218
doi: 10.1007/978-1-4939-7531-0_17
Zhang C, Yu W-Q, Hoshino A et al (2019) Development of ON and OFF cholinergic amacrine cells in the retina. J Comp Neurol 527:174–186
pubmed: 29405294
doi: 10.1002/cne.24405