Phox2b, congenital central hypoventilation syndrome and the control of respiration

Seminars in Cell and Developmental Biology

Volumn 21, Issue 8, 2010, Pages 814-822

  Goridis, Christo ^a,b   Dubreuil, Véronique ^a,b   Thoby Brisson, Muriel ^c   Fortin, Gilles ^c   Brunet, Jean François ^a,b  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b PSL RESEARCH UNIVERSITY   (France)

^c CNRS   (France)

Author keywords

Breathing; Congenital central hypoventilation syndrome; Phox2b; Retrotrapezoid nucleus

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PHOX2B; UNCLASSIFIED DRUG;

ADRENERGIC SYSTEM; ANIMAL MODEL; BRAIN DEVELOPMENT; CONGENITAL CENTRAL HYPOVENTILATION SYNDROME; EMBRYO; GENE EXPRESSION; GENE MUTATION; HIRSCHSPRUNG DISEASE; HYPOVENTILATION; MEDULLA OBLONGATA; MOUSE; NERVE CELL NETWORK; NONHUMAN; RESPIRATION CONTROL; RESPIRATORY NERVE CELL; RETROTRAPEZOID NUCLEUS; REVIEW; RHOMBENCEPHALON; SEROTONINERGIC NERVE CELL;

MAMMALIA;

EID: 78049295515     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2010.07.006     Document Type: Review

References (72)

1. Feldman J.L., Mitchell G.S., Nattie E.E. Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci 2003, 26:239-266.
2. Alheid G.F., McCrimmon D.R. The chemical neuroanatomy of breathing. Respir Physiol Neurobiol 2008, 164:3-11.
3. Smith J.C., Abdala A.P., Rybak I.A., Paton J.F. Structural and functional architecture of respiratory networks in the mammalian brainstem. Philos Trans R Soc Lond B Biol Sci 2009, 364:2577-2587.
4. Thoby-Brisson M., Trinh J.B., Champagnat J., Fortin G. Emergence of the pre-Bötzinger respiratory rhythm generator in the mouse embryo. J Neurosci 2005, 25:4307-4318.
5. Katz D.M., Dutschmann M., Ramirez J.M., Hilaire G. Breathing disorders in Rett syndrome: progressive neurochemical dysfunction in the respiratory network after birth. Respir Physiol Neurobiol 2009, 168:101-108.
6. Nixon G.M., Brouillette R.T. Sleep and breathing in Prader-Willi syndrome. Pediatr Pulmonol 2002, 34:209-217.
7. Gaultier C., Gallego J. Development of respiratory control: evolving concepts and perspectives. Respir Physiol Neurobiol 2005, 149:3-15.
8. Smith J.C., Ellenberger H.H., Ballanyi K., Richter D.W., Feldman J.L. PreBötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 1991, 254:726-729.
9. Feldman J.L., Del Negro C.A. Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 2006, 7:232-242.
10. Tan W., Janczewski W.A., Yang P., Shao X.M., Callaway E.M., Feldman J.L. Silencing preBötzinger complex somatostatin-expressing neurons induces persistent apnea in awake rat. Nat Neurosci 2008, 11:538-540.
11. Guyenet P.G., Bayliss D.A., Stornetta R.L., Fortuna M.G., Abbott S.B., DePuy S.D. Retrotrapezoid nucleus, respiratory chemosensitivity and breathing automaticity. Respir Physiol Neurobiol 2009, 168:59-68.
12. Onimaru H., Ikeda K., Kawakami K. Phox2b, RTN/pFRG neurons and respiratory rhythmogenesis. Respir Physiol Neurobiol 2009, 168:13-18.
13. Smith J.C., Morrison D.E., Ellenberger H.H., Otto M.R., Feldman J.L. Brainstem projections to the major respiratory neuron populations in the medulla of the cat. J Comp Neurol 1989, 281:69-96.
14. Mulkey D.K., Stornetta R.L., Weston M.C., Simmons J.R., Parker A., Bayliss D.A., et al. Respiratory control by ventral surface chemoreceptor neurons in rats. Nat Neurosci 2004, 7:1360-1369.
15. Onimaru H., Homma I. A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 2003, 23:1478-1486.
16. Thoby-Brisson M., Karlén M., Wu N., Charnay P., Champagnat J., Fortin G. Genetic identification of an embryonic parafacial oscillator coupling to the pre-Bötzinger complex. Nature Neurosci 2009, 12:1208-1235.
17. Guyenet P.G., Mulkey D.K. Retrotrapezoid nucleus and parafacial respiratory group. Respir Physiol Neurobiol 2010, 24.
18. 2 homeostasis, and breathing automaticity. J Appl Physiol 2008, 105:404-416.
19. Nattie E., Li A. Central chemoreception is a complex system function that involves multiple brain stem sites. J Appl Physiol 2009, 106:1464-1466.
20. 2 chemoreception. Respir Physiol Neurobiol 2009, 168:49-58.
21. 2 chemoreception and thermoregulation. J Appl Physiol 2010, 108:1425-1432.
22. Buchanan G.F., Richerson G.B. Role of chemoreceptors in mediating dyspnea. Respir Physiol Neurobiol 2009, 167:9-19.
23. Teppema L.J., Dahan A. The ventilatory response to hypoxia in mammals: mechanisms, measurement, and analysis. Physiol Rev 2010, 90:675-754.
24. American Thoracic Society Idiopathic congenital hypoventilation syndrome: diagnosis and management. Am J Resp Crit Care Med 1999, 160:368-373.
25. Weese-Mayer D.E., Berry-Kravis E.M., Ceccherini I., Keens T.G., Loghmanee D.A., Trang H. An official ATS clinical policy statement: congenital central hypoventilation syndrome: genetic basis, diagnosis, and management. Am J Respir Crit Care Med 2010, 181:626-644.
26. Trang H., Dehan M., Beaufils F., Zaccaria I., Amiel J., Gaultier C. The French congenital central hypoventilation syndrome registry: general data, phenotype, and genotype. Chest 2005, 127:72-79.
27. Amiel J., Laudier B., Attie-Bitach T., Trang H., de Pontual L., Gener B., et al. Polyalanine expansion and frameshift mutations of the paired-like homeobox gene PHOX2B in congenital central hypoventilation syndrome. Nat Genet 2003, 33:459-461.
28. Weese-Mayer D.E., Silvestri J.M., Menzies L.J., Morrow-Kenny A.S., Hunt C.E., Hauptman S.A. Congenital central hypoventilation syndrome: diagnosis, management, and long-term outcome in thirty-two children. J Pediatr 1992, 120:381-387.
29. Spengler C.M., Gozal D., Shea S.A. Chemoreceptive mechanisms elucidated by studies of congenital central hypoventilation syndrome. Respir Physiol 2001, 129:247-255.
30. Weese-Mayer D.E., Berry-Kravis E.M., Zhou L. Adult identified with congenital central hypoventilation syndrome-mutation in PHOX2b gene and late-onset CHS. Am J Respir Crit Care Med 2005, 171:88.
31. Trochet D., de Pontual L., Straus C., Gozal D., Trang H., Landrieu P., et al. PHOX2B germline and somatic mutations in late-onset central hypoventilation syndrome. Am J Respir Crit Care Med 2008, 177:906-911.
32. Weese-Mayer D.E., Berry-Kravis E.M., Marazita M.L. In pursuit (and discovery) of a genetic basis for congenital central hypoventilation syndrome. Respir Physiol Neurobiol 2005, 149:73-82.
33. Amiel J., Dubreuil V., Ramanantsoa N., Fortin G., Gallego J., Brunet J.-F., et al. PHOX2B in respiratory control: lessons from congenital central hypoventilation syndrome and its mouse models. Respir Physiol Neurobiol 2009, 168:125-132.
34. Trochet D., O'Brien L.M., Gozal D., Trang H., Nordenskjold A., Laudier B., et al. PHOX2B genotype allows for prediction of tumor risk in congenital central hypoventilation syndrome. Am J Hum Genet 2005, 76:421-426.
35. Parodi S., Bachetti T., Lantieri F., Di Duca M., Santamaria G., Ottonello G., et al. Parental origin and somatic mosaicism of PHOX2B mutations in Congenital Central Hypoventilation Syndrome. Hum Mutat 2008, 29:206.
36. Matera I., Bachetti T., Puppo F., Di Duca M., Morandi F., Casiraghi G.M., et al. PHOX2B mutations and polyalanine expansions correlate with the severity of the respiratory phenotype and associated symptoms in both congenital and late onset Central Hypoventilation syndrome. J Med Genet 2004, 41:373-380.
37. Trochet D., Hong S.J., Lim J.K., Brunet J.-F., Munnich A., Kim K.S., et al. Molecular consequences of PHOX2B missense, frameshift and alanine expansion mutations leading to autonomic dysfunction. Hum Mol Genet 2005, 14:3697-3708.
38. Bachetti T., Matera I., Borghini S., Di Duca M., Ravazzolo R., Ceccherini I. Distinct pathogenetic mechanisms for PHOX2B associated polyalanine expansions and frameshift mutations in congenital central hypoventilation syndrome. Hum Mol Genet 2005, 14:1815-1824.
39. Benailly H.K., Lapierre J.M., Laudier B., Amiel J., Attie T., De Blois M.C., et al. PMX2B, a new candidate gene for Hirschsprung's disease. Clin Genet 2003, 64:204-209.
40. Kumar R., Macey P.M., Woo M.A., Alger J.R., Keens T.G., Harper R.M. Neuroanatomic deficits in congenital central hypoventilation syndrome. J Comp Neurol 2005, 487:361-371.
41. Kumar R., Ahdout R., Macey P.M., Woo M.A., Avedissian C., Thompson P.M., et al. Reduced caudate nuclei volumes in patients with congenital central hypoventilation syndrome. Neuroscience 2009, 163:1373-1379.
42. 2 chemosensitivity, fatal central apnea, and specific loss of parafacial neurons. Proc Natl Acad Sci USA 2008, 105:1067-1072.
43. Pattyn A., Morin X., Cremer H., Goridis C., Brunet J.-F. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 1999, 399:366-370.
44. Pattyn A., Hirsch M.-R., Goridis C., Brunet J.-F. Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development 2000, 127:1349-1358.
45. Blessing W.W. Breathing. The lower brainstem and bodily homeostasis 1997, Oxford University Press, p. 101-164.
46. Brunet J.-F., Pattyn A. Phox2 genes-from patterning to connectivity. Curr Opin Genet Dev 2002, 12:435-440.
47. Brunet J.-F., Goridis C. Phox2b and the homeostatic brain. Genetic basis for respiratory control diseases 2008, 25-38. Springer. C. Gaultier (Ed.).
48. Dauger S., Pattyn A., Lofaso F., Gaultier C., Goridis C., Gallego J., et al. Phox2b controls the development of peripheral chemoreceptors and afferent visceral pathways. Development 2003, 130:6635-6642.
49. Pattyn A., Goridis C., Brunet J.-F. Specification of the central noradrenergic phenotype by the homeobox gene Phox2b. Mol Cell Neurosci 2000, 15:235-243.
50. Stornetta R.L. Neurochemistry of bulbospinal presympathetic neurons of the medulla oblongata. J Chem Neuroanat 2009, 38:222-230.
51. Coppola E., Pattyn A., Guthrie S.C., Goridis C., Studer M. Reciprocal gene replacements reveal unique functions for Phox2 genes during neural differentiation. EMBO J 2005, 24:4392-4403.
52. Kang B.J., Chang D.A., Mackay D.D., West G.H., Moreira T.S., Takakura A.C., et al. Central nervous system distribution of the transcription factor Phox2b in the adult rat. J Comp Neurol 2007, 503:627-641.
53. Ogren J.A., Macey P.M., Kumar R., Woo M.A., Harper R.M. Central autonomic regulation in congenital central hypoventilation syndrome. Neuroscience 2010, 167:1249-1256.
54. Durand E., Dauger S., Pattyn A., Gaultier C., Goridis C., Gallego J. Sleep-disordered breathing in newborn mice heterozygous for the transcription factor Phox2b. Am J Respir Crit Care Med 2005, 172.
55. Stornetta R.L., Moreira T.S., Takakura A.C., Kang B.J., Chang D.A., West G.H., et al. Expression of Phox2b by brainstem neurons involved in chemosensory intergration in the adult rat. J Neurosci 2006, 26:10305-10314.
56. 2 sensitivity in rats. Respir Physiol 1994, 97:63-77.
57. Nattie E.E., Li A. Substance P-saporin lesion of neurons with NK1 receptors in one chemoreceptor site in rats decreases ventilation and chemosensitivity. J Physiol 2002, 544:603-616.
58. Lazarenko R.M., Milner T.A., Depuy S.D., Stornetta R.L., West G.H., Kievits J.A., et al. Acid sensitivity and ultrastructure of the retrotrapezoid nucleus in Phox2b-EGFP transgenic mice. J Comp Neurol 2009, 517:69-86.
59. Dubreuil V., Thoby-Brisson M., Rallu M., Persson K., Pattyn A., Birchmeier C., et al. Defective respiratory rhythmogenesis and loss of central chemosensitivity in Phox2b mutants targeting retrotrapezoid nucleus neurons. J Neurosci 2009, 29:14836-14846.
60. Rose M.F., Ren J., Ahmad K.A., Chao H.T., Klisch T.J., Flora A., et al. Math1 is essential for the development of hindbrain neurons critical for perinatal breathing. Neuron 2009, 64:341-354.
61. 2-sensitive neurons in rats. J Physiol 2006, 572:503-523. Epub 2006 Feb 2002.
62. Sieber M.A., Storm R., Martinez-de-la-Torre M., Muller T., Wende H., Reuter K., et al. Lbx1 acts as a selector gene in the fate determination of somatosensory and viscerosensory relay neurons in the hindbrain. J Neurosci 2007, 27:4902-4909.
63. Schneider-Maunoury S., Topilko P., Seitanidou T., Levi G., Cohen-Tannoudji M., Pournin S., et al. Disruption of Krox-20 results in alteration of rhombomeres 3 and 5 in the developing hindbrain. Cell 1993, 75:1199-1214.
64. Voiculescu O., Charnay P., Schneider-Maunoury S. Expression pattern of a Krox-20/Cre knock-in allele in the developing hindbrain, bones, and peripheral nervous system. Genesis 2000, 26:123-126.
65. Pagliardini S., Ren J., Gray P.A., Vandunk C., Gross M., Goulding M., et al. Central respiratory rhythmogenesis is abnormal in lbx1- deficient mice. J Neurosci 2008, 28:11030-11041.
66. 2-sensitive preinspiratory neurons of the parafacial respiratory group express Phox2b in the neonatal rat. J Neurosci 2008, 28:12845-12850.
67. Pattyn A., Vallstedt A., Dias J.M., Samad O.A., Krumlauf R., Rijli F.M., et al. Coordinated temporal and spatial control of motor neuron and serotonergic neuron generation from a common pool of CNS progenitors. Genes Dev 2003, 17:729-737.
68. Mulkey D.K., Rosin D.L., West G., Takakura A.C., Moreira T.S., Bayliss D.A., et al. Serotonergic neurons activate chemosensitive retrotrapezoid nucleus neurons by a pH-independent mechanism. J Neurosci 2007, 27:14128-14138.
69. Jacquin T.D., Borday V., Schneider-Maunoury S., Topilko P., Ghilini G., Kato F., et al. Reorganization of pontine rhythmogenic neuronal networks in Krox-20 knockout mice. Neuron 1996, 17:747-758.
70. Awatramani R., Soriano P., Rodriguez C., Mai J.J., Dymecki S.M. Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation. Nat Genet 2003, 35:70-75.
71. Paterson D.S., Thompson E.G., Kinney H.C. Serotonergic and glutamatergic neurons at the ventral medullary surface of the human infant: observations relevant to central chemosensitivity in early human life. Auton Neurosci 2006, 124:112-124.
72. Rudzinski E., Kapur R.P. PHOX2B immunolocalization of the candidate human retrotrapezoid nucleus. Pediatr Dev Pathol 2009, 4:4.