Dysphagia and disrupted cranial nerve development in a mouse model of DiGeorge (22q11) deletion syndrome

DMM Disease Models and Mechanisms

Volumn 7, Issue 2, 2014, Pages 245-257

  Karpinski, Beverly A ^a   Maynard, Thomas M ^a   Fralish, Matthew S ^a   Nuwayhid, Samer ^a,b   Zohn, Irene E ^a,b   Moody, Sally A ^a   LaMantia, Anthony S ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

Cranial nerve development; DiGeorge 22q11 deletion syndrome; Dysphagia; Hindbrain patterning

Indexed keywords

RETINOIC ACID; T BOX TRANSCRIPTION FACTOR; TBX1 PROTEIN, MOUSE;

ANIMAL; ANIMAL EMBRYO; CHROMOSOME DELETION; CRANIAL NERVE; CRANIOFACIAL MALFORMATION; DIGEORGE SYNDROME; DISEASE MODEL; DYSPHAGIA; EMBRYOLOGY; FEEDING BEHAVIOR; FEMALE; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MORPHOGENESIS; MOUSE; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; SWALLOWING;

ANIMALS; ANIMALS, NEWBORN; BODY PATTERNING; CHROMOSOME DELETION; CRANIAL NERVES; CRANIOFACIAL ABNORMALITIES; DEGLUTITION; DEGLUTITION DISORDERS; DIGEORGE SYNDROME; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; FEEDING BEHAVIOR; FEMALE; GENE DOSAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; PHENOTYPE; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TRETINOIN;

EID: 84894351786     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.012484     Document Type: Article

References (64)

1. Abu-Abed, S. S., Beckett, B. R., Chiba, H., Chithalen, J. V., Jones, G., Metzger, D., Chambon, P. and Petkovich, M. (1998). Mouse P450RAI (CYP26) expression and retinoic acid-inducible retinoic acid metabolism in F9 cells are regulated by retinoic acid receptor gamma and retinoid X receptor alpha. J. Biol. Chem. 273, 2409-2415.
2. Ang, K. K., McRitchie, R. J., Minson, J. B., Llewellyn-Smith, I. J., Pilowsky, P. M., Chalmers, J. P. and Arnolda, L. F. (1999). Activation of spinal opioid receptors contributes to hypotension after hemorrhage in conscious rats. Am. J. Physiol. 276, H1552-H1558.
3. Arnold, J. S., Werling, U., Braunstein, E. M., Liao, J., Nowotschin, S., Edelmann, W., Hebert, J. M. and Morrow, B. E. (2006). Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development 133, 977-987.
4. Balcombe, N. R. (1999). Dysphagia and hypercalcaemia. Postgrad. Med. J. 75, 373-374.
5. Barrow, J. R., Stadler, H. S. and Capecchi, M. R. (2000). Roles of Hoxa1 and Hoxa2 in patterning the early hindbrain of the mouse. Development 127, 933-944.
6. Bennetto, L., Kuschner, E. S. and Hyman, S. L. (2007). Olfaction and taste processing in autism. Biol. Psychiatry 62, 1015-1021.
7. Braunstein, E. M., Monks, D. C., Aggarwal, V. S., Arnold, J. S. and Morrow, B. E. (2009). Tbx1 and Brn4 regulate retinoic acid metabolic genes during cochlear morphogenesis. BMC Dev. Biol. 9, 31.
8. Calmont, A., Ivins, S., Van Bueren, K. L., Papangeli, I., Kyriakopoulou, V., Andrews, W. D., Martin, J. F., Moon, A. M., Illingworth, E. A., Basson, M. A. et al. (2009). Tbx1 controls cardiac neural crest cell migration during arch artery development by regulating Gbx2 expression in the pharyngeal ectoderm. Development 136, 3173-3183.
9. Cayé-Thomasen, P. and Tos, M. (2003). Eustachian tube goblet cell density during and after acute otitis media caused by Streptococcus pneumoniae: a morphometric analysis. Otol. Neurotol. 24, 365-370.
10. Christensen, J. R. (1989). Developmental approach to pediatric neurogenic dysphagia. Dysphagia 3, 131-134.
11. Cordes, S. P. (2001). Molecular genetics of cranial nerve development in mouse. Nat. Rev. Neurosci. 2, 611-623.
12. Eicher, P. S., McDonald-Mcginn, D. M., Fox, C. A., Driscoll, D. A., Emanuel, B. S. and Zackai, E. H. (2000). Dysphagia in children with a 22q11.2 deletion: unusual pattern found on modified barium swallow. J. Pediatr. 137, 158-164.
13. Emanuel, B. S., McDonald-McGinn, D., Saitta, S. C. and Zackai, E. H. (2001). The 22q11.2 deletion syndrome. Adv. Pediatr. 48, 39-73.
14. Friedman, M. A., Miletta, N., Roe, C., Wang, D., Morrow, B. E., Kates, W. R., Higgins, A. M. and Shprintzen, R. J. (2011). Cleft palate, retrognathia and congenital heart disease in velo-cardio-facial syndrome: a phenotype correlation study. Int. J. Pediatr. Otorhinolaryngol. 75, 1167-1172.
15. Fukui, N., Amano, A., Akiyama, S., Daikoku, H., Wakisaka, S. and Morisaki, I. (2000). Oral findings in DiGeorge syndrome: clinical features and histologic study of primary teeth. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 89, 208-215.
16. Glover, J. C., Renaud, J. S. and Rijli, F. M. (2006). Retinoic acid and hindbrain patterning. J. Neurobiol. 66, 705-725.
17. Grieve, R. J. and Dixon, P. F. (1983). Dysphagia: a further symptom of hypercalcaemia? Br. Med. J. 286, 1935-1936.
18. Guris, D. L., Duester, G., Papaioannou, V. E. and Imamoto, A. (2006). Dosedependent interaction of Tbx1 and Crkl and locally aberrant RA signaling in a model of del22q11 syndrome. Dev. Cell 10, 81-92.
19. Hernandez, R. E., Putzke, A. P., Myers, J. P., Margaretha, L. and Moens, C. B. (2007). Cyp26 enzymes generate the retinoic acid response pattern necessary for hindbrain development. Development 134, 177-187.
20. Hopkin, R. J., Schorry, E. K., Bofinger, M. and Saal, H. M. (2000). Increased need for medical interventions in infants with velocardiofacial (deletion 22q11) syndrome. J. Pediatr. 137, 247-249.
21. Huang, R. Y. and Shapiro, N. L. (2000). Structural airway anomalies in patients with DiGeorge syndrome: a current review. Am. J. Otolaryngol. 21, 326-330.
22. Jadcherla, S. R., Vijayapal, A. S. and Leuthner, S. (2009). Feeding abilities in neonates with congenital heart disease: a retrospective study. J. Perinatol. 29, 112-118.
23. Jawad, A. F., McDonald-Mcginn, D. M., Zackai, E. and Sullivan, K. E. (2001). Immunologic features of chromosome 22q11.2 deletion syndrome (DiGeorge syndrome/velocardiofacial syndrome). J. Pediatr. 139, 715-723.
24. Jerome, L. A. and Papaioannou, V. E. (2001). DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat. Genet. 27, 286-291.
25. Kelly, M. M. (2006). Primary care issues for the healthy premature infant. J. Pediatr. Health Care 20, 293-299.
26. Kobrynski, L. J. and Sullivan, K. E. (2007). Velocardiofacial syndrome, DiGeorge syndrome: the chromosome 22q11.2 deletion syndromes. Lancet 370, 1443-1452.
27. Kubilus, J. K. and Linsenmayer, T. F. (2010). Developmental guidance of embryonic corneal innervation: roles of Semaphorin 3 A and Slit2. Dev. Biol. 344, 172-184.
28. Lefton-Greif, M. A. (2008). Pediatric dysphagia. Phys. Med. Rehabil. Clin. N. Am. 19, 837-851 ix. (ix.).
29. Lima, K., Foølling, I., Eiklid, K. L., Natvig, S. and Abrahamsen, T. G. (2010). Agedependent clinical problems in a Norwegian national survey of patients with the 22q11.2 deletion syndrome. Eur. J. Pediatr. 169, 983-989.
30. Lundy, D. S., Smith, C., Colangelo, L., Sullivan, P. A., Logemann, J. A., Lazarus, C. L., Newman, L. A., Murry, T., Lombard, L. and Gaziano, J. (1999). Aspiration: cause and implications. Otolaryngol. Head Neck Surg. 120, 474-478.
31. Ma, L. and Tessier-Lavigne, M. (2007). Dual branch-promoting and branch-repelling actions of Slit/Robo signaling on peripheral and central branches of developing sensory axons. J. Neurosci. 27, 6843-6851.
32. Marom, T., Roth, Y., Goldfarb, A. and Cinamon, U. (2012). Head and neck manifestations of 22q11.2 deletion syndromes. Eur. Arch. Otorhinolaryngol. 269, 381-387.
33. Marshall, H., Nonchev, S., Sham, M. H., Muchamore, I., Lumsden, A. and Krumlauf, R. (1992). Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature 360, 737-741.
34. Maynard, T. M., Haskell, G. T., Bhasin, N., Lee, J. M., Gassman, A. A., Lieberman, J. A. and LaMantia, A. S. (2002). RanBP1, a velocardiofacial/DiGeorge syndrome candidate gene, is expressed at sites of mesenchymal/epithelial induction. Mech. Dev. 111, 177-180.
35. Maynard, T. M., Haskell, G. T., Peters, A. Z., Sikich, L., Lieberman, J. A. and LaMantia, A. S. (2003). A comprehensive analysis of 22q11 gene expression in the developing and adult brain. Proc. Natl. Acad. Sci. USA 100, 14433-14438.
36. Maynard, T. M., Gopalakrishna, D., Meechan, D. W., Paronett, E. M., Newbern, J. M. and LaMantia, A. S. (2013). 22q11 Gene dosage establishes an adaptive range for sonic hedgehog and retinoic acid signaling during early development. Hum. Mol. Genet. 22, 300-312.
37. Meechan, D. W., Tucker, E. S., Maynard, T. M. and LaMantia, A. S. (2009). Diminished dosage of 22q11 genes disrupts neurogenesis and cortical development in a mouse model of 22q11 deletion/DiGeorge syndrome. Proc. Natl. Acad. Sci. USA 106, 16434-16445.
38. Merscher, S., Funke, B., Epstein, J. A., Heyer, J., Puech, A., Lu, M. M., Xavier, R. J., Demay, M. B., Russell, R. G., Factor, S. et al. (2001). TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 104, 619-629.
39. Mic, F. A., Haselbeck, R. J., Cuenca, A. E. and Duester, G. (2002). Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development 129, 2271-2282.
40. Monks, D. C. and Morrow, B. E. (2012). Identification of putative retinoic acid target genes downstream of mesenchymal Tbx1 during inner ear development. Dev. Dyn. 241, 563-573.
41. Okano, J., Sakai, Y. and Shiota, K. (2008). Retinoic acid down-regulates Tbx1 expression and induces abnormal differentiation of tongue muscles in fetal mice. Dev. Dyn. 237, 3059-3070.
42. Okano, J., Kimura, W., Papaionnou, V. E., Miura, N., Yamada, G., Shiota, K. and Sakai, Y. (2012). The regulation of endogenous retinoic acid level through CYP26B1 is required for elevation of palatal shelves. Dev. Dyn. 241, 1744-1756.
43. Ousley, O., Rockers, K., Dell, M. L., Coleman, K. and Cubells, J. F. (2007). A review of neurocognitive and behavioral profiles associated with 22q11 deletion syndrome: implications for clinical evaluation and treatment. Curr. Psychiatry Rep. 9, 148-158.
44. Phelan, E., Ryan, S. and Rowley, H. (2011). Vascular rings and slings: interesting vascular anomalies. J. Laryngol. Otol. 125, 1158-1163.
45. Philipp, U., Menzel, J. and Distl, O. (2011). A rare form of persistent right aorta arch in linkage disequilibrium with the DiGeorge critical region on CFA26 in German Pinschers. J. Hered. 102 Suppl. 1, S68-S73.
46. Raft, S., Nowotschin, S., Liao, J. and Morrow, B. E. (2004). Suppression of neural fate and control of inner ear morphogenesis by Tbx1. Development 131, 1801-1812.
47. Reijntjes, S., Gale, E. and Maden, M. (2003). Expression of the retinoic acid catabolising enzyme CYP26B1 in the chick embryo and its regulation by retinoic acid. Gene Expr. Patterns 3, 621-627.
48. Reilly, S. M., Skuse, D. H., Wolke, D. and Stevenson, J. (1999). Oral-motor dysfunction in children who fail to thrive: organic or non-organic? Dev. Med. Child Neurol. 41, 115-122.
49. Richtsmeier, J. T., Baxter, L. L. and Reeves, R. H. (2000). Parallels of craniofacial maldevelopment in Down syndrome and Ts65Dn mice. Dev. Dyn. 217, 137-145.
50. Roberts, C., Ivins, S., Cook, A. C., Baldini, A. and Scambler, P. J. (2006). Cyp26 genes a1, b1 and c1 are down-regulated in Tbx1 null mice and inhibition of Cyp26enzyme function produces a phenocopy of DiGeorge Syndrome in the chick. Hum. Mol. Genet. 15, 3394-3410.
51. Rommel, N., Davidson, G., Cain, T., Hebbard, G. and Omari, T. (2008). Videomanometric evaluation of pharyngo-oesophageal dysmotility in children with velocardiofacial syndrome. J. Pediatr. Gastroenterol. Nutr. 46, 87-91.
52. Ruda, J. M., Krakovitz, P. and Rose, A. S. (2012). A review of the evaluation and management of velopharyngeal insufficiency in children. Otolaryngol. Clin. North Am. 45, 653-669, viii. (viii.).
53. Scambler, P. J. (2010). 22q11 deletion syndrome: a role for TBX1 in pharyngeal and cardiovascular development. Pediatr. Cardiol. 31, 378-390.
54. Schwarz, S. M., Corredor, J., Fisher-Medina, J., Cohen, J. and Rabinowitz, S. (2001). Diagnosis and treatment of feeding disorders in children with developmental disabilities. Pediatrics 108, 671-676.
55. Shiau, C. E. and Bronner-Fraser, M. (2009). N-cadherin acts in concert with Slit1- Robo2 signaling in regulating aggregation of placode-derived cranial sensory neurons. Development 136, 4155-4164.
56. Shiau, C. E., Lwigale, P. Y., Das, R. M., Wilson, S. A. and Bronner-Fraser, M. (2008). Robo2-Slit1 dependent cell-cell interactions mediate assembly of the trigeminal ganglion. Nat. Neurosci. 11, 269-276.
57. Sobin, C., Kiley-Brabeck, K., Dale, K., Monk, S. H., Khuri, J. and Karayiorgou, M. (2006). Olfactory disorder in children with 22q11 deletion syndrome. Pediatrics 118, e697-e703.
58. Tahayato, A., Dollé, P. and Petkovich, M. (2003). Cyp26C1 encodes a novel retinoic acid-metabolizing enzyme expressed in the hindbrain, inner ear, first branchial arch and tooth buds during murine development. Gene Expr. Patterns 3, 449-454.
59. Tarquinio, D. C., Jones, M. C., Jones, K. L. and Bird, L. M. (2012). Growth charts for 22q11 deletion syndrome. Am. J. Med. Genet. A. 158A, 2672-2681.
60. Tavassoli, T. and Baron-Cohen, S. (2012). Taste identification in adults with autism spectrum conditions. J. Autism Dev. Disord. 42, 1419-1424.
61. Trainor, P. A. and Krumlauf, R. (2000). Patterning the cranial neural crest: hindbrain segmentation and Hox gene plasticity. Nat. Rev. Neurosci. 1, 116-124.
62. Trinick, R., Johnston, N., Dalzell, A. M. and McNamara, P. S. (2012). Reflux aspiration in children with neurodisability - a significant problem, but can we measure it? J. Pediatr. Surg. 47, 291-298.
63. Vitelli, F., Morishima, M., Taddei, I., Lindsay, E. A. and Baldini, A. (2002). Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum. Mol. Genet. 11, 915-922.
64. Zori, R. T., Boyar, F. Z., Williams, W. N., Gray, B. A., Bent-Williams, A., Stalker, H. J., Rimer, L. A., Nackashi, J. A., Driscoll, D. J., Rasmussen, S. A. et al. (1998). Prevalence of 22q11 region deletions in patients with velopharyngeal insufficiency. Am. J. Med. Genet. 77, 8-11.