Hirschsprung-like disease is exacerbated by reduced de novo GMP synthesis

Journal of Clinical Investigation

Volumn 123, Issue 11, 2013, Pages 4875-4887

  Lake, Jonathan I ^a   Tusheva, Olga A ^a   Graham, Brittany L ^a   Heuckeroth, Robert O ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTESUNATE; BENZBROMARONE; CINCHOPHEN; CLOSANTEL; DICLAZURIL; FLUBENDAZOLE; GUANINE NUCLEOTIDE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; MEVINOLIN; MYCOPHENOLIC ACID; OXIBENDAZOLE; PURINE;

AGANGLIONOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOSYNTHESIS; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE EXACERBATION; DISEASE SEVERITY; DNA SYNTHESIS; FEMALE; HIRSCHSPRUNG DISEASE; INTESTINE INNERVATION; LAMELLIPODIUM; MOSAICISM; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NONHUMAN; PENETRANCE; PRECURSOR; PRIORITY JOURNAL; X CHROMOSOME INACTIVATION; ZEBRA FISH;

EID: 84887499789     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI69781     Document Type: Article

References (65)

1. Heuckeroth RO. Hirschsprung disease. In: Faure C, Di Lorenzo C, Thapar N, eds. Pediatric Neurogastroenterology. New York, New York, USA: Humana Press; 2013:271-283.
2. Amiel J, et al. Hirschsprung disease, associated syndromes and genetics: a review. J Med Genet. 2008; 45(1):1-14.
3. Carrasquillo MM, McCallion AS, Puffenberger EG, Kashuk CS, Nouri N, Chakravarti A. Genome-wide association study and mouse model identify interaction between RET and EDNRB pathways in Hirschsprung disease. Nat Genet. 2002;32(2):237-244.
4. Gabriel SB, et al. Segregation at three loci explains familial and population risk in Hirschsprung disease. Nat Genet. 2002;31(1):89-93.
5. Emison ES, et al. A common sex-dependent mutation in a RET enhancer underlies Hirschsprung disease risk. Nature. 2005;434(7035):857-863.
6. de Pontual L, et al. Epistatic interactions with a common hypomorphic RET allele in syndromic Hirschsprung disease. Hum Mutat. 2007;28(8):790-796.
7. Heanue TA, Pachnis V. Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies. Nat Rev Neurosci. 2007;8(6):466-479.
8. Fu M, Tam PKH, Sham MH, Lui VCH. Embryonic development of the ganglion plexuses and the concentric layer structure of human gut: a topographical study. Anat Embryol. 2004;208(1):33-41.
9. Wallace AS, Burns AJ. Development of the enteric nervous system, smooth muscle and interstitial cells of Cajal in the human gastrointestinal tract. Cell Tissue Res. 2005;319(3):367-382.
10. Lake JI, Heuckeroth RO. Enteric nervous system development: migration, differentiation, and disease. Am J Physiol Gastrointest Liver Physiol. 2013; 305(1):G1-G24.
11. Vohra BPS, Fu M, Heuckeroth RO. Protein kinase Cζ and glycogen synthase kinase-3β control neuronal polarity in developing rodent enteric neurons, whereas SMAD specific E3 ubiquitin protein ligase 1 promotes neurite growth but does not influence polarity. J Neurosci. 2007;27(35):9458-9468.
12. Fu M, et al. Vitamin A facilitates enteric nervous system precursor migration by reducing Pten accumulation. Development. 2010;137(4):631-640.
13. Stewart AL, Young HM, Popoff M, Anderson RB. Effects of pharmacological inhibition of small GTPases on axon extension and migration of enteric neural crest-derived cells. Dev Biol. 2007; 307(1):92-104.
14. Zhang Y, Kim T-H, Niswander L. Phactr4 regulates directional migration of enteric neural crest through PP1, integrin signaling, and cofilin activity. Genes Dev. 2012;26(1):69-81.
15. Anderson RB, Turner KN, Nikonenko AG, Hemperly J, Schachner M, Young HM. The cell adhesion molecule L1 is required for chain migration of neural crest cells in the developing mouse gut. Gastroenterology. 2006;130(4):1221-1232.
16. Breau MA, Dahmani A, Broders-Bondon F, Thiery J-P, Dufour S. β1 integrins are required for the invasion of the caecum and proximal hindgut by enteric neural crest cells. Development. 2009;136(16):2791-2801.
17. Broders-Bondon F, Paul-Gilloteaux P, Carlier C, Radice GL, Dufour S. N-cadherin and β1-integrins cooperate during the development of the enteric nervous system. Dev Biol. 2012;364(2):178-191.
18. Chong CR, Chen X, Shi L, Liu JO, Sullivan DJ. A clinical drug library screen identifies astemizole as an antimalarial agent. Nat Chem Biol. 2006;2(8):415-416.
19. Kuhlman J, Eisen JS. Genetic screen for mutations affecting development and function of the enteric nervous system. Dev Dyn. 2007;236(1):118-127.
20. Genentech Inc. CellCept. Genentech Web site. http://www.gene.com/ download/pdf/cellcept-prescribing.pdf. Accessed August 28, 2013.
21. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2008;22(3):659-661.
22. Sato Y, Heuckeroth RO. Retinoic acid regulates murine enteric nervous system precursor proliferation, enhances neuronal precursor differentiation, and reduces neurite growth in vitro. Dev Biol. 2008; 320(1):185-198.
23. Jonsson CA, Svensson L, Carlsten H. Beneficial effect of the inosine monophosphate dehydrogenase inhibitor mycophenolate mofetil on survival and severity of glomerulonephritis in systemic lupus erythematosus (SLE)-prone MRLlpr/lpr mice. Clin Exp Immunol. 1999;116(3):534-541.
24. Corpening JC, Deal KK, Cantrell VA, Skelton SB, Buehler DP, Southard-Smith EM. Isolation and live imaging of enteric progenitors based on Sox10-Histone2BVenus transgene expression. Genesis. 2011; 49(7):599-618.
25. Wallace AS, Schmidt C, Schachner M, Wegner M, Anderson RB. L1cam acts as a modifier gene during enteric nervous system development. Neurobiol Dis. 2010;40(3):622-633.
26. Uesaka T, Nagashimada M, Yonemura S, Enomoto H. Diminished Ret expression compromises neuronal survival in the colon and causes intestinal aganglionosis in mice. J Clin Invest. 2008; 118(5):1890-1898.
27. Simpson MJ, Zhang DC, Mariani M, Landman KA, Newgreen DF. Cell proliferation drives neural crest cell invasion of the intestine. Dev Biol. 2007; 302(2):553-568.
28. Hooper M, Hardy K, Handyside A, Hunter S, Monk M. HPRT-deficient (Lesch-Nyhan) mouse embryos derived from germline colonization by cultured cells. Nature. 1987;326(6110):292-295.
29. Allison AC, Eugui EM. Mycophenolate mofetil and its mechanisms of action. Immunopharmacology. 2000;47(2-3):85-118.
30. Hadjantonakis AK, Cox LL, Tam PP, Nagy A. An X-linked GFP transgene reveals unexpected paternal X-chromosome activity in trophoblastic giant cells of the mouse placenta. Genesis. 2001;29(3):133-140.
31. Anderka MT, Lin AE, Abuelo DN, Mitchell AA, Rasmussen SA. Reviewing the evidence for mycophenolate mofetil as a new teratogen: Case report and review of the literature. Am J Med Genet. 2009; 149A(6):1241-1248.
32. Lin AE, Singh KE, Strauss A, Nguyen S, Rawson K, Kimonis VE. An additional patient with mycophenolate mofetil embryopathy: cardiac and facial analyses. Am J Med Genet A. 2011;155A(4):748-756.
33. Britsch S, et al. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev. 2001;15(1):66-78.
34. Paratore C, Eichenberger C, Suter U, Sommer L. Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease. Hum Mol Genet. 2002;11(24):3075-3085.
35. Young HM, et al. Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev Biol. 2004;270(2):455-473.
36. Natarajan D, Marcos-Gutierrez C, Pachnis V, de Graaff E. Requirement of signalling by receptor tyrosine kinase RET for the directed migration of enteric nervous system progenitor cells during mammalian embryogenesis. Development. 2002; 129(22):5151-5160.
37. Gianino S, Grider JR, Cresswell J, Enomoto H, Heuckeroth RO. GDNF availability determines enteric neuron number by controlling precursor proliferation. Development. 2003;130(10):2187-2198.
38. Jain S, et al. Mice expressing a dominant-negative Ret mutation phenocopy human Hirschsprung disease and delineate a direct role of Ret in spermatogenesis. Development. 2004;131(21):5503-5513.
39. Kapur RP, Yost C, Palmiter RD. A transgenic model for studying development of the enteric nervous system in normal and aganglionic mice. Development. 1992;116(1):167.
40. Druckenbrod NR, Epstein ML. Age-dependent changes in the gut environment restrict the invasion of the hindgut by enteric neural progenitors. Development. 2009;136(18):3195-3203.
41. Hotta R, Anderson RB, Kobayashi K, Newgreen DF, Young HM. Effects of tissue age, presence of neurones and endothelin-3 on the ability of enteric neurone precursors to colonize recipient gut: implications for cell-based therapies. Neurogastroenterol Motil. 2010;22(3):331-e86.
42. Curry CJ, et al. Smith-Lemli-Opitz syndrome-type II: multiple congenital anomalies with male pseudohermaphroditism and frequent early lethality. Am J Med Genet. 1987;26(1):45-57.
43. Barlow AJ, Dixon J, Dixon MJ, Trainor PA. Balancing neural crest cell intrinsic processes with those of the microenvironment in Tcof1 haploinsufficient mice enables complete enteric nervous system formation. Hum Mol Genet. 2012;21(8):1782-1793.
44. Long H, Cameron S, Yu L, Rao Y. De novo GMP synthesis is required for axon guidance in Drosophila. Genetics. 2006;172(3):1633-1642.
45. Schmidt F, Eckardt K, Shakibaei M, Glander P, Stahlmann R. Effects of mycophenolic acid alone and in combination with its metabolite mycophenolic acid glucuronide on rat embryos in vitro. Arch Toxicol. 2013;87(2):361-370.
46. Mondin M, Moreau V, Genot E, Combe C, Ripoche J, Dubus I. Alterations in cytoskeletal protein expression by mycophenolic acid in human mesangial cells requires Rac inactivation. Biochem Pharmacol. 2007;73(9):1491-1498.
47. Krotz F, et al. Mycophenolate acid inhibits endothelial NAD(P)H oxidase activity and superoxide formation by a Rac1-dependent mechanism. Hypertension. 2007;49(1):201-208.
48. Kapur RP, Livingston R, Doggett B, Sweetser DA, Siebert JR, Palmiter RD. Abnormal microenvironmental signals underlie intestinal aganglionosis in dominant megacolon mutant mice. Dev Biol. 1996; 174(2):360-369.
49. Kapur RP, Sweetser DA, Doggett B, Siebert JR, Palmiter RD. Intercellular signals downstream of endothelin receptor-B mediate colonization of the large intestine by enteric neuroblasts. Development. 1995;121(11):3787-3795.
50. Carmona-Fontaine C, et al. Complement fragment C3a controls mutual cell attraction during collective cell migration. Developmental Cell. 2011; 21(6):1026-1037.
51. Carmona-Fontaine C, et al. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature. 2008;456(7224):957-961.
52. Wang X, Chan AKK, Sham M-H, Burns AJ, Chan WY. Analysis of the sacral neural crest cell contribution to the hindgut enteric nervous system in the mouse embryo. Gastroenterology. 2011;141(3):992-1002.e6.
53. Anderson RB. Matrix metalloproteinase-2 is involved in the migration and network formation of enteric neural crest-derived cells. Int J Dev Biol. 2010;54(1):63-69.
54. Murphey RD, Zon LI. Small molecule screening in the zebrafish. Methods. 2006;39(3):255-261.
55. Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP. Modification of gene activity in mouse embryos in utero by a tamoxifeninducible form of Cre recombinase. Curr Biol. 1998; 8(24):1323-1326.
56. Srinivas S, et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol. 2001;1:4.
57. Enomoto H, Crawford PA, Gorodinsky A, Heuckeroth RO, Johnson EM Jr, Milbrandt J. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development. 2001;128(20):3963-3974.
58. Stratman JL, Barnes WM, Simon TC. Universal PCR genotyping assay that achieves single copy sensitivity with any primer pair. Transgenic Res. 2003; 12(4):521-522.
59. Creedon DJ, et al. Neurturin shares receptors and signal transduction pathways with glial cell line-derived neurotrophic factor in sympathetic neurons. Proc Natl Acad Sci USA. 1997;94(13):7018-7023.
60. Vohra BP, Planer W, Armon J, Fu M, Jain S, Heuckeroth RO. Reduced endothelin converting enzyme-1 and endothelin-3 mRNA in the developing bowel of male mice may increase expressivity and penetrance of Hirschsprung disease-like distal intestinal aganglionosis. Dev Dyn. 2007;236(1):106-117.
61. Wang H, Zhang Y, Heuckeroth RO. PAI-1 deficiency reduces liver fibrosis after bile duct ligation in mice through activation of tPA. FEBS Lett. 2007; 581(16):3098-3104.
62. Ramakers C, Ruijter JM, Deprez RHL, Moorman AF. Assumption-free analysis of quantitative realtime polymerase chain reaction (PCR) data. Neurosci Lett. 2003;339(1):62-66.
63. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29(9):e45.
64. Preibisch S, Saalfeld S, Tomancak P. Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics. 2009;25(11):1463-1465.
65. Meijering E, Dzyubachyk O, Smal I. Methods for cell and particle tracking. Methods Enzymol. 2012; 504:183-200.