Analyses with double knockouts of the Bmpr1a and Bmpr1b genes demonstrate that BMP signaling is involved in the formation of precerebellar mossy fiber nuclei derived from the rhombic lip


Autoři: Lihua Qin aff001;  Kyung J. Ahn aff001;  Lara Wine Lee aff001;  Charles de Charleroy, Jr aff001;  E. Bryan Crenshaw, III aff001
Působiště autorů: Division of Pediatric Otolaryngology, Mammalian Neurogenetics Group, Center for Childhood Communication, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States of America aff001;  Department of Anatomy and Histoembryology, School of Basic Medical Sciences, Peking University Health Science Center, Beijing, China aff002;  Neuroscience Graduate Group, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America aff003;  Department of Otorhinolaryngology, Head and Neck Surgery, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226602

Souhrn

Bone morphogenetic proteins (BMPs) have been hypothesized to specify distinct dorsal neural fates. During neural development, BMPs are expressed in the roof plate and adjacent neuroepithelium. Because several hindbrain nuclei that form the proprioceptive/vestibular/auditory sensory network originate from the rhombic lip, near the roof plate, BMP signaling may regulate the development of these nuclei. To test this hypothesis genetically, we have examined the development of the hindbrain in BMP type I receptor knockout mice. Our results demonstrate that BMP signaling is involved in the formation of precerebellar mossy fiber nuclei, which give rise to cerebellar mossy fibers, but is not required for the development of the inferior olivary nucleus, which gives rise to cerebellar climbing fibers.

Klíčová slova:

Auditory pathway – BMP signaling – Cerebellum – Gene expression – Nerve fibers – Neurons – Hindbrain – Climbing fibers


Zdroje

1. Wingate R.J., Hatten M.E., 1999. The role of the rhombic lip in avian cerebellum development. Development 126, 4395–4404. 10498676

2. Wullimann M.F., Mueller T., Distel M., Babaryka A., Grothe B., Koster R.W. (2011). The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis. Front. Neuroanat. 5, 27. doi: 10.3389/fnana.2011.00027 21559349

3. Kratochwil CF, Maheshwari U and Rijli FM (2017). The Long Journey of Pontine Nuclei Neurons: From Rhombic lip to Cortico-Ponto-Cerebellar Circuitry. Front. Neural Circuits 11, 33.

4. Alder J., Lee K.J., Jessell T.M., Hatten M.E., 1999. Generation of cerebellar granule neurons in vivo by transplantation of BMP-treated neural progenitor cells. Nat. Neurosci. 2, 535–540. doi: 10.1038/9189 10448218

5. Hallonet M.E., Teillet M.A., Le Douarin N.M., 1990. A new approach to the development of the cerebellum provided by the quail-chick marker system. Development 108, 19–31. 2351063

6. Machold R., Fishell G., 2005. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors.[see comment]. Neuron 48, 17–24. doi: 10.1016/j.neuron.2005.08.028 16202705

7. Zhang L., Goldman J.E., 1996. Developmental fates and migratory pathways of dividing progenitors in the postnatal rat cerebellum. Journal of Comparative Neurology 370, 536–550. doi: 10.1002/(SICI)1096-9861(19960708)370:4<536::AID-CNE9>3.0.CO;2-5 8807453

8. Altman J., and Bayer S. A. (1987a). Development of the precerebellar nuclei in the rat: I. The precerebellar neuroepithelium of the rhombencephalon. J. Comp. Neurol. 257, 477–489. doi: 10.1002/cne.902570402 3693594

9. Altman J., and Bayer S. A. (1987b). Development of the precerebellar nuclei in the rat: II. The intramural olivary migratory stream and the neurogenetic organization of the inferior olive. J. Comp. Neurol. 257, 490–512. doi: 10.1002/cne.902570403 3693595

10. Altman J., and Bayer S. A. (1987c). Development of the precerebellar nuclei in the rat: III. The posterior precerebellar extramural migratory stream and the lateral reticular and external cuneate nuclei. J. Comp. Neurol. 257, 513–528. doi: 10.1002/cne.902570404 3693596

11. Altman J., and Bayer S. A. (1987d). Development of the precerebellar nuclei in the rat: IV. The anterior precerebellar extramural migratory stream and the nucleus reticularis tegmenti pontis and the basal pontine gray. J. Comp. Neurol. 257, 529–552. doi: 10.1002/cne.902570405 3693597

12. Essik C.R., 1912. The development of the nuclei pontis and nucleus arcuatus in man. Am. J. Anat. 13.

13. His, W., 1891. Die Entwicklung des menschlichen Rautenhirns vom Ende des ersten bis zum Beginn des dritten Monats. I. Verlängertes Mark. Abhandlung der königlicher sächsischen Gesellschaft der Wissenschaften, Mathematische-physikalische Klasse 20.

14. Rodriguez C. I., and Dymecki S. M. (2000). Origin of the precerebellar system. Neuron 27, 475–486. doi: 10.1016/s0896-6273(00)00059-3 11055431

15. Landsberg R.L., Awatramani R.B., Hunter N.L., Farago A.F., DiPietrantonio H.J., Rodriguez C.I., Dymecki S.M., 2005. Hindbrain rhombic lip is comprised of discrete progenitor cell populations allocated by Pax6. Neuron 48, 933–947. doi: 10.1016/j.neuron.2005.11.031 16364898

16. Ben-Arie N., Bellen H.J., Armstrong D.L., McCall A.E., Gordadze P.R., Guo Q., et al., 1997. Math1 is essential for genesis of cerebellar granule neurons. Nature 390, 169–172. doi: 10.1038/36579 9367153

17. Wang V.Y., Rose M.F., Zoghbi H.Y., 2005. Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48, 31–43. doi: 10.1016/j.neuron.2005.08.024 16202707

18. Hoshino M., Seto Y., Yamada M. (2013) Specification of Cerebellar and Precerebellar Neurons. In: Manto M., Schmahmann J.D., Rossi F., Gruol D.L., Koibuchi N. (eds) Handbook of the Cerebellum and Cerebellar Disorders. Springer, Dordrecht

19. Ben-Arie N., Hassan B.A., Bermingham N.A., Malicki D.M., Armstrong D., Matzuk M., et al., 2000. Functional conservation of atonal and Math1 in the CNS and PNS. Development 127, 1039–1048. 10662643

20. Fujiyama T., Yamada M., Terao M., Terashima T., Hioki H., Inoue Y.U., et al., 2009. Inhibitory and excitatory subtypes of cochlear nucleus neurons are defined by distinct bHLH transcription factors, Ptf1a and Atoh1. Development 136, 2049–2058. doi: 10.1242/dev.033480 19439493

21. Hoshino M., Nakamura S., Mori K., Kawauchi T., Terao M., Nishimura Y.V., et al., 2005. Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 47, 201–213. doi: 10.1016/j.neuron.2005.06.007 16039563

22. Storm R., Cholewa-Waclaw J., Reuter K., Brohl D., Sieber M., Treier M., et al. 2009. The bHLH transcription factor Olig3 marks the dorsal neuroepithelium of the hindbrain and is essential for the development of brainstem nuclei. Development 136, 295–305. doi: 10.1242/dev.027193 19088088

23. Yamada M., Terao M., Terashima T., Fujiyama T., Kawaguchi Y., Nabeshima Y., et al. 2007. Origin of climbing fiber neurons and their developmental dependence on Ptf1a. Journal of Neuroscience 27, 10924–10934. doi: 10.1523/JNEUROSCI.1423-07.2007 17928434

24. Dun XP (2012) Origin of climbing fiber neurons and the definition of rhombic lip. Int J Dev Neurosci 30, 391–395. doi: 10.1016/j.ijdevneu.2012.02.002 22406199

25. Liu A., Niswander L.A., 2005. Bone morphogenetic protein signalling and vertebrate nervous system development. [Review] [117 refs]. Nature Reviews Neuroscience 6, 945–954. doi: 10.1038/nrn1805 16340955

26. Tong KK, Ma TC, Kwan KM. BMP/Smad signaling and embryonic cerebellum development: stem cell specification and heterogeneity of anterior rhombic lip. Dev Growth Differ 2015;57:121–34. doi: 10.1111/dgd.12198 25705796

27. Hogan B.L., 1996. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes & Development 10, 1580–1594.

28. Pogue R., Lyons K., 2006. BMP signaling in the cartilage growth plate. [Review] [232 refs]. Current Topics in Developmental Biology 76, 1–48. doi: 10.1016/S0070-2153(06)76001-X 17118262

29. Hegarty S.V., O'Keeffe G.W., Sullivan A.M., 2013. BMP-Smad 1/5/8 signalling in the development of the nervous system. Prog Neurobiol 109, 28–41. doi: 10.1016/j.pneurobio.2013.07.002 23891815

30. Le Dreau G., Marti E., 2013. The multiple activities of BMPs during spinal cord development. Cell Mol Life Sci 70, 4293–4305. doi: 10.1007/s00018-013-1354-9 23673983

31. Massague J., 1996. TGFbeta signaling: receptors, transducers, and Mad proteins. Cell 85, 947–950. doi: 10.1016/s0092-8674(00)81296-9 8674122

32. Miyazono K., Maeda S., Imamura T., 2005. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. [Review] [130 refs]. Cytokine & Growth Factor Reviews 16, 251–263.

33. ten Dijke P., Miyazono K., Helden C.-H., 1996. Signaling via heterooligomeric complexes of type I and type II serine/threonine kinase receptors. Curr Opin Cell Biol. 8, 139–145. doi: 10.1016/s0955-0674(96)80058-5 8791413

34. Zeng S., Chen J., Shen H., 2010. Controlling of bone morphogenetic protein signaling. Cellular Signalling 22, 888–893. doi: 10.1016/j.cellsig.2009.12.007 20060893

35. Zhao G.Q., 2003. Consequences of knocking out BMP signaling in the mouse. Genesis 35, 43–56. doi: 10.1002/gene.10167 12481298

36. Dewulf N, Verschueren K, Lonnoy O, Morén A, Grimsby S, Vande Spiegle K, et al. 1995 Distinct spatial and temporal expression patterns of two type I receptors for bone morphogenetic proteins during mouse embryogenesis. Endocrinology 136, 2652–2663. doi: 10.1210/endo.136.6.7750489 7750489

37. Panchision DM1, Pickel JM, Studer L, Lee SH, Turner PA, Hazel TG, et al. (2001) Sequential actions of BMP receptors control neural precursor cell productionand fate. Genes Dev. 15(16), 2094–110. doi: 10.1101/gad.894701 11511541

38. Ahn K., Mishina Y., Hanks M.C., Behringer R.R., Crenshaw E.B. 3rd, 2001. BMPR-IA signaling is required for the formation of the apical ectodermal ridge and dorsal-ventral patterning of the limb. Development 128, 4449–4461. 11714671

39. Mishina Y., Hanks M.C., Miura S., Tallquist M.D., Behringer R.R., 2002. Generation of Bmpr/Alk3 conditional knockout mice. Genesis: the Journal of Genetics & Development. 32, 69–72.

40. Wine-Lee L., Ahn K.J., Richardson R.D., Mishina Y., Lyons K.M., Crenshaw E.B. III, 2004. Signaling through BMP type 1 receptors is required for development of interneuron cell types in the dorsal spinal cord. Development 131, 5393–5403. doi: 10.1242/dev.01379 15469980

41. Yi S.E., Daluiski A., Pederson R., Rosen V., Lyons K.M., 2000. The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 127, 621–630. 10631182

42. Soriano P., 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genetics 21, 70–71. doi: 10.1038/5007 9916792

43. Wilkinson D.G. (Ed.), 1992. In situ hybridization: a practical approach. Oxford University Press, New York.

44. Sieber MA, Storm R, Martinez-de-la-Torre M, Müller T, Wende H, Reuter K, Vasyutina E, Birchmeier C., 2007. Lbx1 Acts as a Selector Gene in the Fate Determination of Somatosensory and Viscerosensory Relay Neurons in the Hindbrain. J. Neurosci. 27, 4902–4909. doi: 10.1523/JNEUROSCI.0717-07.2007 17475798

45. Phippard D., Lu L., Lee D., Saunders J.C., Crenshaw E.B. III, 1999. Targeted mutagenesis of the POU-domain gene, Brn4/Pou3f4, causes development defects in the inner ear. J. Neurosci. 19, 5980–5989. doi: 10.1523/JNEUROSCI.19-14-05980.1999 10407036

46. Qin L., Wine-Lee L., Ahn K.J., Crenshaw E.B. 3rd, 2006. Genetic analyses demonstrate that bone morphogenetic protein signaling is required for embryonic cerebellar development. Journal of Neuroscience 26, 1896–1905. doi: 10.1523/JNEUROSCI.3202-05.2006 16481421

47. Chizhikov V.V., Millen K.J., 2005. Roof plate-dependent patterning of the vertebrate dorsal central nervous system. [Review] [60 refs]. Developmental Biology 277, 287–295. doi: 10.1016/j.ydbio.2004.10.011 15617675

48. Lee K.J., Mendelsohn M., Jessell T.M., 1998. Neuronal patterning by BMPs: a requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord. Genes & Development 12, 3394–3407.

49. Lee K.J., Dietrich P., Jessell T.M., 2000. Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification [see comments]. Nature 403, 734–740. doi: 10.1038/35001507 10693795

50. Parras C.M., Schuurmans C., Scardigli R., Kim J., Anderson D.J., Guillemot F., 2002. Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes & Development 16, 324–338.

51. Li S., Qiu F., Xu A., Price S. M., and Xiang M. (2004). Barhl1 regulates migration and survival of cerebellar granule cells by controlling expression of the neurotrophin-3 gene. J. Neurosci. 24, 3104–3114. doi: 10.1523/JNEUROSCI.4444-03.2004 15044550

52. Aruga J., Minowa O., Yaginuma H., Kuno J., Nagai T., Noda T., et al. 1998. Mouse Zic1 is involved in cerebellar development. J. Neurosci. 18, 284–293. doi: 10.1523/JNEUROSCI.18-01-00284.1998 9412507

53. Aruga J., Inoue T., Hoshino J., Mikoshiba K., 2002. Zic2 controls cerebellar development in cooperation with Zic1. Journal of Neuroscience 22, 218–225. doi: 10.1523/JNEUROSCI.22-01-00218.2002 11756505

54. Foletti DL and Scheller RH (2001) Developmental regulation and specific brain distribution of phosphorabphilin. J Neurosci 21, 5461–5472. doi: 10.1523/JNEUROSCI.21-15-05461.2001 11466417

55. Logan C.Y., Nusse R., 2004. The Wnt signaling pathway in development and disease. [Review] [196 refs]. Annual Review of Cell & Developmental Biology 20, 781–810.

56. Montcouquiol M., Crenshaw E.B. III, Kelley M.W., 2006. Non-Canonical Wnt Signaling and Neural Polarity. Ann. Rev. Neurosci. 28, 363–386.

57. Nusse R., 2005. Wnt signaling in disease and in development. [Review] [42 refs]. Cell Research 15, 28–32. doi: 10.1038/sj.cr.7290260 15686623

58. Hollyday M., McMahon J.A., McMahon A.P., 1995. Wnt expression patterns in chick embryo nervous system. Mechanisms of Development 52, 9–25. doi: 10.1016/0925-4773(95)00385-e 7577679

59. Parr B.A., Shea M.J., Vassileva G., McMahon A.P., 1993. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119, 247–261. 8275860

60. Hunter N. L. & Dymecki S. M. (2007) Molecularly and temporally separable lineages form the hindbrain roof plate and contribute differentially to the choroid plexus. Development 134, 3449–3460. doi: 10.1242/dev.003095 17728348

61. Marin F., Puelles L., 1995. Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. European Journal of Neuroscience 7, 1714–1738. doi: 10.1111/j.1460-9568.1995.tb00693.x 7582126

62. Okada T., Keino-Masu K., Masu M., 2007. Migration and nucleogenesis of mouse precerebellar neurons visualized by in utero electroporation of a green fluorescent protein gene. Neuroscience Research 57, 40–49. doi: 10.1016/j.neures.2006.09.010 17084476

63. Kawabata M., Inoue H., Hanyu A., Imamura T., Miyazono K., 1998. Smad proteins exist as monomers in vivo and undergo homo- and hetero-oligomerization upon activation by serine/threonine kinase receptors. EMBO Journal 17, 4056–4065. doi: 10.1093/emboj/17.14.4056 9670020

64. Yamada M., Seto Y., Taya S., Owa T., Inoue Y. U., Inoue T., et al. (2014). Specification of spatial identities of cerebellar neuron progenitors by Ptf1A and Atoh1 for proper production of GABAergic and glutamatergic neurons. J. Neurosci. 34, 4786–4800. doi: 10.1523/JNEUROSCI.2722-13.2014 24695699

65. Dickinson M.E., Krumlauf R., McMahon A.P., 1994. Evidence for a mitogenic effect of Wnt-1 in the developing mammalian central nervous system. Development 120, 1453–1471. 8050356

66. Ikeya M., Lee S.M., Johnson J.E., McMahon A.P., Takada S., 1997. Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389, 966–970. doi: 10.1038/40146 9353119

67. Megason S.G., McMahon A.P., 2002. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087–2098. 11959819

68. Ciani L., Salinas P.C., 2005. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. [Review] [137 refs][Erratum appears in Nat Rev Neurosci. 2005 Jul;6(7):582]. Nature Reviews Neuroscience 6, 351–362.

69. Garcin C.L, Habib S.J. (2017) A Comparative Perspective on Wnt/β-Catenin Signalling in Cell Fate Determination. In: Tassan JP., Kubiak J. (eds) Asymmetric Cell Division in Development, Differentiation and Cancer. Results and Problems in Cell Differentiation, vol 61. Springer, Cham.

70. Zechner D., Müller T., Wende H., Walther I., Taketo M. M., Crenshaw E. B., et al. (2007). Bmp and Wnt/beta-catenin signals control expression of the transcription factor Olig3 and the specification of spinal cord neurons. Dev. Biol. 303, 181–190. doi: 10.1016/j.ydbio.2006.10.045 17150208

71. Muroyama Y., Fujihara M., Ikeya M., Kondoh H., Takada S., 2002. Wnt signaling plays an essential role in neuronal specification of the dorsal spinal cord. Genes & Development 16, 548–553.

72. Shi F, Cheng YF, Wang XL, Edge AS (2010). Beta-catenin up-regulates Atoh1 expression in neural progenitor cells by interaction with an Atoh1 3′ enhancer. J Biol Chem. 285, 392–400. doi: 10.1074/jbc.M109.059055 19864427

73. Marcelle C., Stark M.R., Bronner-Fraser M., 1997. Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124, 3955–3963. 9374393

74. Chizhikov VV, Lindgren AG, Currle D, Rose M, Monuki ES, Millen KJ (2006). The roof plate regulates cerebellar cell-type specification and proliferation. Development 133: 2793–804. doi: 10.1242/dev.02441 16790481


Článek vyšel v časopise

PLOS One


2019 Číslo 12