Ret deficiency in mice impairs the development of A5 and A6 neurons and the functional maturation of the respiratory rhythm

European Journal of Neuroscience

Volumn 22, Issue 10, 2005, Pages 2403-2412

  Viemari, J C ^a,e   Maussion, G ^b   Bevengut M ^a   Burnet, H ^a   Pequignot, J M ^c   Nepote V ^b   Pachnis, V ^d   Simonneau, M ^b   Hilaire, G ^a  

^a CNRS   (France)

^b HÔPITAL ROBERT DEBRÉ   (France)

^c UNIVERSITÉ LYON 1   (France)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

Catecholaminergic system; Fetal; Network activity; Respiratory system

Indexed keywords

NORADRENALIN; PROTEIN RET; TYROSINE 3 MONOOXYGENASE; TYROSINE KINASE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; FEMALE; FETUS; GESTATIONAL AGE; HETEROZYGOSITY; HYPOXIA; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; LIQUID CHROMATOGRAPHY; MEDULLA OBLONGATA; MOUSE; NERVE CELL; NONHUMAN; PONS; PONS ANGLE; PRIORITY JOURNAL; RESPIRATORY SYSTEM;

ANIMALS; BIOGENIC MONOAMINES; BRAIN STEM; FEMALE; GENOTYPE; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE NET; NEURONS; NOREPINEPHRINE; PONS; PREGNANCY; PROTO-ONCOGENE PROTEINS C-RET; RESPIRATORY MECHANICS; RESPIRATORY SYSTEM; RHOMBENCEPHALON; RNA, MESSENGER;

EID: 28744446441     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04441.x     Document Type: Article

References (45)

1. Achard, P., Zanella, S., Rodriguez, R. & Hilaire, G. (2005) Perinatal maturation of the respiratory rhythm generator in mammals: from experimental results to computational simulation. Resp. Physiol. Neurobiol., 149, 17-27.
2. Aizenfisz, S., Dauger, S., Durand, E., Vardon, G., Levacher, B., Simonneau, M., Pachnis, V., Gaultier, C. & Gallego, J. (2002) Ventilatory responses to hypercapnia and hypoxia in heterozygous c-Ret newborn mice. Respir. Physiol. Neurobiol., 131, 213-222.
3. Al Halabiah, H., Delezoide, A.L., Cardona, A., Moalic, J.M. & Simonneau, M. (2005) Expression pattern of NOGO and NgR genes during human development. Gene Expr. Patterns, 5, 561-568.
4. Barlow, A., de Graaff, E. & Pachnis, V. (2003) Enteric nervous system progenitors are coordinately controlled by the G protein-coupled receptor EDNRB and the receptor tyrosine kinase. RET. Neuron, 40, 905-916.
5. Blanchi, B., Kelly, L.M., Viemari, J.C., Lafon, I., Burner, H., Bevengut, M., Tillmanns, S., Daniel, L., Graft, T., Hilaire, G. & Sieweke, M.H. (2003) MafB deficiency causes defective respiratory rhythmogenesis and fatal central apnea at birth. Nat. Neurosci., 6, 1091-1100.
6. Blanchi, B. & Sieweke, M.H. (2005) Mutations of brainstem transcription factors and central respiratory disorders. Trends Mol. Med., 11, 23-30.
7. Bou-Flores, C., Lajard, A.M., Monteau, R., De Maeyer, E., Seif, I., Lanoir, J. & Hilaire, G. (2000) Abnormal phrenic motoneurone activity and morphology in neonatal monoamine oxidase A-deficient transgenic mice, possible role of serotonin excess. J. Neurosci., 20, 4646-4656.
8. Cransac, H., Cottet-Emard, J.M., Pequignot, J.M. & Peyrin, L. (1996) Monoamines (norepinephrine, dopamine, serotonin) in the rat medial vestibular nucleus, endogenous levels and turnover. J. Neural Transm., 103, 391-401.
9. Dauger, S., Guimiot, F., Renolleau, S., Levacher, B., Boda, B., Mas, C., Nepote, V., Simonneau, M., Gaultier, C. & Gallego, J. (2001) MASH-1/RET pathway involvement in development of brain stem control of respiratory frequency in newborn mice. Physiol. Genomics, 7, 149-157.
10. Dobbins, E. & Feldman, J. (1994) Brainstem network controlling descending drive to phrenic motoneurons in rat. J. Comp. Neurol., 347, 64-86.
11. Errchidi, S., Hilaire, G. & Monteau, R. (1990) Permanent release of noradrenaline modulates respiratory frequency in the newborn rat, an in vitro study. J. Physiol. (Lond.), 429, 497-510.
12. Errchidi, S., Hilaire, G. & Monteau, R. (1991) Noradrenergic modulation of the medullary respiratory rhythm generator in the newborn rat, an in vitro study. J. Physiol. (Lond.), 443, 477-498.
13. Gaultier, C., Amiel, J., Dauger, S., Trang, H., Lyonnet, S., Gallego, J. & Simonneau, M. (2004) Genetics and early disturbances of breathing control. Pediatr. Res., 55, 729-733.
14. Gaytan, S., Pasaro, R., Coulon, P., Bévengut, M. & Hilaire, G. (2002) Identification of central nervous system neurons innervating the respiratory muscles of the mouse, a transneuronal tracing study. Brain Res. Bull., 57, 335-339.
15. Goridis, C. & Rohrer, H. (2002) Specification of catecholaminergic and serotonergic neurons. Nat. Rev. Neurosci., 3, 531-541.
16. Grimm, J., Mueller, A., Hefti, F. & Rosenthal, A. (2004) Molecular basis for catecholaminergic neuron diversity. Proc. Natl. Acad. Sci. USA, 101, 13891-13896.
17. Guo, H., Hellard, D.T., Huang, L. & Katz, D. (2005) Development of pontine noradrenergic A5 neurons requires brain-derived neurotrophic factor. Eur. J. Neurosci., 21, 2019-2023.
18. Hilaire, G. & Pasaro, R. (2003) Genesis and control of the respiratory rhythm in adult mammals. News Physiol. Sci., 18, 23-28.
19. Hilaire, G., Viemari, J.C., Coulon, P., Simonneau, M. & Bevengut, M. (2004) Modulation of the respiratory rhythm generator by the pontine noradrenergic A5 and A6 groups in rodents. Respir. Physiol. Neurobiol., 143, 187-197.
20. Hirsch, M., Tiveron, M.C., Guillemot, F., Brunet, J.F. & Goridis, C. (1998) Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development, 125, 599-608.
21. Holm, P.C., Rodriguez, F.J., Kresse, A., Canals, J.M., Silos-Santiago, I. & Arenas, E. (2003) Crucial role of TrkB ligands in the survival and phenotypic differentiation of developing locus coeruleus noradrenergic neurons. Development, 130, 3535-3545.
22. Huang, L., Guo, H., Hellard, D.T. & Katz, D.M. (2005) Glial cell line-derived neurotrophic factor (GDNF) is required for differentiation of pontine noradrenergic neurons and patterning of central respiratory output. Neuroscience, 130, 95-105.
23. Kato, T., Hayashi, F., Tatsumi, K., Kuriyama, T. & Fukuda, Y. (2000) Inhibitory mechanisms in hypoxic respiratory depression studied in an in vitro preparation. Neurosci. Res., 38, 281-288.
24. Kawai, A., Okada, Y., Muckenhoff, K. & Scheid, P. (1995) Theophylline and hypoxic ventilatory response in the rat isolated brainstem-spinal cord. Respir. Physiol., 100, 25-32.
25. Lo, L., Tiveron, M.C. & Anderson, D. (1998) MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples panneuronal and subtype-specific components of autonomic neuronal identity. Development, 125, 609-620.
26. Morin, X., Cremer, H., Hirsch, M.R., Kapur, R.P., Goridis, C. & Brunet, J.F. (1997) Defects in sensory and autonomic ganglia and absence of locus coeruleus in mice deficient for the homeobox gene Phox2a. Neuron, 18, 411-423.
27. Natarajan, D., Marcos-Gutierrez, C., Pachnis, V. & de Graaff, E. (2002) Requirement of signalling by receptor tyrosine kinase RET for the directed migration of enteric nervous system progenitor cells during mammalian embryogenesis. Development, 129, 5151-5160.
28. Pachnis, V., Mankoo, B. & Costantini, F. (1993) Expression of the c-Ret protooncogene during mouse embryogenesis. Development, 119, 1005-1017.
29. Pattyn, A., Goridis, C. & Brunet, J.F. (2000) Specification of the central noradrenergic phenotype by the homeobox gene Phox2b. Mol. Cell Neurosci., 15, 235-243.
30. Pattyn, A., Morin, X., Cremer, H., Goridis, C. & Brunet, J.F. (1997) Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development, 124, 4065-4075.
31. Pattyn, A., Morin, X., Cremer, H., Goridis, C. & Brunet, J.F. (1999) The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature, 399, 366-370.
32. Patlyn, A., Simplicio, N., Van Doorninck, J.H., Goridis, C., Guillemot, F. & Brunet, J.F. (2004) Ascii/Mash1 is required for the development of central serotonergic neurons. Nat. Neurosci., 1, 589-595.
33. Qian, Y, Fritzsch, B., Shirasawa, S., Chen, C.L., Choi, Y. & Ma, Q. (2001) Formation of brainstem (nor) adrenergic centers and first-order relay visceral sensory neurons is dependent on homeodomain protein Rnx/Tlx3. Genes Dev., 15, 2533-2545.
34. Qian, Y., Shirasawa, S., Chen, C., Cheng, L. & Ma, Q. (2002) Proper development of relay somatic sensory neurons and D2/D4 interneurons requires homeobox genes Rnx/Tlx-3 and Tlx-1. Genes Dev., 16, 1220-1233.
35. Schuchardt, A., D'Agati, V., Larsson-Blomberg, L., Costantini, F. & Pachnis, V. (1994) Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature, 367, 380-383.
36. Shirasawa, S., Arata, A., Onimaru, H., Roth, K., Brown, G., Horning, S., Arata, S., Okumura, K., Sasazuki, T. & Kormeyer, S. (2000) Rnx deficiency results in congenital central hypoventilation. Nat. Genet., 24, 287-290.
37. Steindler, D.A. & Trosko, B.K. (1989) Two types of locus coeruleus neurons born on different embryonic days in the mouse. Anat. Embryol. (Berl.), 179, 423-434.
38. Suzue, T. (1984) Respiratory rhythm generation in the in vitro brainstem-spinal cord preparation of the neonatal rat. J. Physiol. (Lond.), 354, 173-183.
39. Thomas, S., Matsumoto, A. & Palmiter, R. (1995) Noradrenaline is essential for mouse fetal development. Nature, 374, 643-646.
40. Tiveron, M.C., Hirsch, M.R. & Brunet, J.F. (1996) The expression pattern of the transcription factor Phox2 delineates synaptic palhways of the autonomic nervous system. J. Neurosci., 16, 7649-7660.
41. Ungerstedt, U. (1971) Stereotaxic mapping of the monoamine pathways in the rat brain. Acta Physiol. Scand. Suppl., 367, 1-48.
42. Viemari, J.C., Bévengut, M., Burnet, H., Coulon, P., Pequignot, J.M., Tiveron, M.C. & Hilaire, G. (2004a) Phox2a gene, A6 neurons and noradrenaline are essential for development of normal respiratory rhythm in mice. J. Neurosci., 24, 928-937.
43. Viemari, J.C., Bevengut, M., Coulon, P. & Hilaire, G. (2004b) Nasal trigeminal inputs release the A5 inhibition received by the respiratory rhythm generator of the mouse neonate. J. Neurophysiol., 91, 746-758.
44. Viemari, J.C., Burnet, H., Bévengut, M. & Hilaire, G. (2003) Perinatal maturation of the mouse respiratory rhythm-generator, in vivo and in vitro studies. Eur. J. Neurosci., 17, 1-12.
45. Viemari, J.C. & Hilaire, G. (2002) Noradrenergic receptors and in vitro respiratory rhythm, possible interspecies differences between mouse and rat neonates. Neurosci. Lett., 324, 149-153.