Exome sequencing identified NRG3 as a novel susceptible gene of Hirschsprung's disease in a Chinese population

Molecular Neurobiology

Volumn 47, Issue 3, 2013, Pages 957-966

  Yang, Jun ^a,d   Duan, Shengyu ^a   Zhong, Rong ^a   Yin, Jieyun ^a   Pu, Jiarui ^a   Ke, Juntao ^a   Lu, Xuzai ^a   Zou, Li ^a   Zhang, Hongmei ^a   Zhu, Zhidong ^b   Wang, Depeng ^c   Xiao, Huasheng ^b   Guo, Anyuan ^a   Xia, Jiahong ^a   Miao, Xiaoping ^a   Tang, Shaotao ^a   Wang, Guobin ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b Key Laboratory of Health and Disease Genomics   (China)

^c Nextomics Biosciences Co Ltd   (China)

^d Wuhan Children's Hospital   (China)

Author keywords

Hirschsprung's disease (HSCR); NRG3; Single nucleotide variants (SNVs); Whole exome sequence

Indexed keywords

ALANINE; GLYCINE; NEU DIFFERENTIATION FACTOR; NEUREGULIN 3; NUCLEOTIDE; THREONINE; UNCLASSIFIED DRUG; NRG3 PROTEIN, HUMAN;

ARTICLE; BIOINFORMATICS; CASE REPORT; CHINESE; EXOME; FEMALE; FILTRATION; FOLLOW UP; GENE SEQUENCE; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HIRSCHSPRUNG DISEASE; HUMAN; MALE; MOTHER; QUALITATIVE ANALYSIS; SEQUENCE ANALYSIS; SON; VALIDATION PROCESS; ALGORITHM; ASIAN; CHINA; DNA SEQUENCE; EXON; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETICS; HUMAN GENOME; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; REPRODUCIBILITY; SINGLE NUCLEOTIDE POLYMORPHISM;

ALGORITHMS; ASIAN CONTINENTAL ANCESTRY GROUP; BASE SEQUENCE; CHINA; EXOME; EXONS; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; GENOME, HUMAN; HIRSCHSPRUNG DISEASE; HUMANS; MALE; MOLECULAR SEQUENCE DATA; NEUREGULINS; OPEN READING FRAMES; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCIBILITY OF RESULTS; SEQUENCE ANALYSIS, DNA;

EID: 84887287147     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-012-8392-4     Document Type: Article

References (40)

1. Iwashita T, Kruger GM, Pardal R, Kiel M.J., Morrison S.J. (2003) Hirschsprung disease is linked to defects in neural crest stem cell function. Science 301(5635):972-976
2. Kenny SE, Tam PK, Garcia-Barcelo M (2010) Hirschsprung's disease. Semin Pediatr Surg 19(3):194-200
3. Amiel J, Sproat-Emison E, Garcia-Barcelo M, Lantieri F, Burzynski G., Borrego S, Pelet A, Arnold S, Miao X, Griseri P, Brooks AS, Antinolo G, de Pontual L, Clement-Ziza M, Munnich A, Kashuk C, West K, Wong KK, Lyonnet S, Chakravarti A, Tam PK, Ceccherini I, Hofstra RM, Fernandez R (2008) Hirschsprung disease, associated syndromes and genetics: a review. J Med Genet 45(1):1-14
4. Garcia-Barcelo M.M., Tang CS, Ngan E.S., Lui VC, Chen Y, So MT, Leon T.Y., Miao XP, Shum CK, Liu FQ, Yeung MY, Yuan ZW, Guo WH, Liu L, Sun XB, Huang LM, Tou JF, Song YQ, Chan D, Cheung KM, Wong KK, Cherny SS, Sham PC, Tam PK (2009) Genome-wide association study identifies NRG1 as a susceptibility locus for Hirschsprung's disease. Proc Natl Acad Sci U S A 106 (8):2694-2699
5. Tam PK, Garcia-Barcelo M (2009) Genetic basis of Hirschsprung's disease. Pediatr Surg Int 25(7):543-558
6. Amiel J, Laudier B, Attie-Bitach T, Trang H., de Pontual L, Gener B, Trochet D., Etchevers H, Ray P, Simonneau M, Vekemans M, Munnich A, Gaultier C, Lyonnet S (2003) Polyalanine expansion and frameshift mutations of the paired-like homeobox gene PHOX2B in congenital central hypoventilation syndrome. Nat Genet 33(4):459-461
7. Wakamatsu N, Yamada Y, Yamada K., Ono T, Nomura N, Taniguchi H., Kitoh H, Mutoh N, Yamanaka T, Mushiake K, Kato K, Sonta S, Nagaya M (2001) Mutations in SIP1, encoding Smad interacting protein-1, cause a form of Hirschsprung disease. Nat Genet 27(4):369-370
8. Puffenberger EG, Hosoda K, Washington S.S., Nakao K., deWit D, Yanagisawa M, Chakravart A. (1994) A missense mutation of the endothelin-B receptor gene in multigenic Hirschsprung's disease. Cell 79(7):1257-1266
9. Hofstra RM, Osinga J, Tan-Sindhunata G, Wu Y., Kamsteeg EJ, Stulp RP, van Ravenswaaij-Arts C, Majoor-Krakauer D, Angrist M, Chakravarti A, Meijers C, Buys CH (1996) A homozygous mutation in the endothelin-3 gene associated with a combined Waardenburg type 2 and Hirschsprung phenotype (Shah-Waardenburg syndrome). Nat Genet 12(4):445-447
10. Edery P, Lyonnet S, Mulligan L.M., Pelet A., Dow E, Abel L, Holder S., Nihoul-Fekete C, Ponder BA, Munnich A (1994) Mutations of the RET proto-oncogene in Hirschsprung's disease. Nature 367 (6461):378-380
11. Garcia-Barcelo M.M., Miao X, Lui V.C., So MT, Ngan ES, Leon TY, Lau D.K., Liu TT, Lao X, Guo W, Holden WT, Moore J, Tam PK (2007) Correlation between genetic variations in Hox clusters and Hirschsprung's disease. Ann Hum Genet 71 (Pt 4):526-536
12. Miao X, Garcia-Barcelo MM, So M.T., Leon TY, Lau DK, Liu TT, Chan E.K., Lan LC, Wong KK, Lui VC, Tam PK (2007) Role of RET and PHOX2B gene polymorphisms in risk of Hirschsprung's disease in Chinese population. Gut 56(5):736
13. Miao X, Leon TY, Ngan E.S., So MT, Yuan ZW, Lui VC, Chen Y, Wong K.K., Tam PK, Garcia-Barcelo M (2010) Reduced RET expression in gut tissue of individuals carrying risk alleles of Hirschsprung's disease. Hum Mol Genet 19(8):1461-1467
14. Emison ES, McCallion AS, Kashuk C.S., Bush RT, Grice E, Lin S, Portnoy M.E., Cutler DJ, Green ED, Chakravarti A (2005) A common sex-dependent mutation in a RET enhancer underlies Hirschsprung disease risk. Nature 434(7035):857-863
15. Tang CS, Sribudiani Y, Miao X.P., de Vries AR, Burzynski G, So MT, Leon Y.Y., Yip BH, Osinga J, Hui KJ, Verheij JB, Cherny SS, Tam PK, Sham PC, Hofstra RM, Garcia-Barcelo MM (2010) Fine mapping of the 9q31 Hirschsprung's disease locus. Hum Genet 127(6):675-683
16. 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(22):5151-5160
17. Emison ES, Garcia-Barcelo M, Grice E.A., Lantieri F., Amiel J, Burzynski G, Fernandez R.M., Hao L., Kashuk C, West K, Miao X, Tam PK, Griseri P, Ceccherini I, Pelet A, Jannot AS, de Pontual L, Henrion-Caude A, Lyonnet S, Verheij JB, Hofstra RM, Antinolo G, Borrego S, McCallion AS, Chakravarti A (2010) Differential contributions of rare and common, coding and noncoding Ret mutations to multifactorial Hirschsprung disease liability. Am J Hum Genet 87(1):60-74
18. Majewski J, Schwartzentruber J, Lalonde E., Montpetit A, Jabado N. (2011) What can exome sequencing do for you? J Med Genet 48 (9):580-589
19. Ng PC, Kirkness E.F. (2010) Whole genome sequencing. Methods Mol Biol 628:215-226
20. Ng SB, Bigham AW, Buckingham K.J., Hannibal MC, McMillin MJ, Gildersleeve HI, Beck A.E., Tabor HK, Cooper GM, Mefford HC, Lee C, Turner EH, Smith JD, Rieder MJ, Yoshiura K, Matsumoto N, Ohta T, Niikawa N, Nickerson DA, Bamshad MJ, Shendure J (2010) Exome sequencing identifies MLL2 mutations as a cause of Kabuki syndrome. Nat Genet 42(9):790-793
21. Adie EA, Adams RR, Evans K.L., Porteous DJ, Pickard B.S. (2005) Speeding disease gene discovery by sequence based candidate prioritization. BMC Bioinforma 6:55
22. Chen J, Bardes EE, Aronow B.J., Jegga A.G. (2009) ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res 37 (Web Server issue):W305-W311
23. Aerts S, Lambrechts D, Maity S., Van Loo P, Coessens B, De Smet F, Tranchevent LC, De Moor B, Marynen P, Hassan B, Carmeliet P, Moreau Y (2006) Gene prioritization through genomic data fusion. Nat Biotechnol 24(5):537-544
24. Dahlquist KD, Salomonis N, Vranizan K., Lawlor SC, Conklin B.R. (2002) GenMAPP, a new tool for viewing and analyzing micro-array data on biological pathways. Nat Genet 31(1):19-20
25. Kanehisa M, Goto S. (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27-30
26. Adzhubei IA, Schmidt S, Peshkin L., Ramensky VE, Gerasimova A, Bork P, Kondrashov A.S., Sunyaev S.R. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7 (4):248-249
27. Britsch S, Goerich DE, Riethmacher D, Peirano R.I., Rossner M., Nave KA, Birchmeier C, Wegner M. (2001) The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 15(1):66-78
28. Crone SA, Negro A, Trumpp A., Giovannini M, Lee K.F. (2003) Colonic epithelial expression of ErbB2 is required for postnatal maintenance of the enteric nervous system. Neuron 37(1):29-40
29. Altshuler D, Daly MJ, Lander E.S. (2008) Genetic mapping in human disease. Science 322(5903):881-888
30. Redon R, Ishikawa S, Fitch K.R., Feuk L., Perry GH, Andrews TD, Fiegler H, Shapero M.H., Carson AR, Chen W, Cho EK, Dallaire S, Freeman JL, Gonzalez JR, Gratacos M, Huang J, Kalaitzopoulos D, Komura D, MacDonald JR, Marshall CR, Mei R, Montgomery L, Nishimura K, Okamura K, Shen F, Somerville MJ, Tchinda J, Valsesia A, Woodwark C, Yang F, Zhang J, Zerjal T, Armengol L, Conrad DF, Estivill X, Tyler-Smith C, Carter NP, Aburatani H, Lee C, Jones KW, Scherer SW, Hurles ME (2006) Global variation in copy number in the human genome. Nature 444(7118):444-454
31. Burns AJ, Pachnis V. (2009) Development of the enteric nervous system: bringing together cells, signals and genes. Neurogastroen-terol Motil 21(2):100-102
32. Lemke G (1996) Neuregulins in development. Mol Cell Neurosci 7 (4):247-262
33. Howard B, Panchal H, McCarthy A., Ashworth A. (2005) Identification of the scaramanga gene implicates Neuregulin3 in mammary gland specification. Genes Dev 19(17):2078-2090
34. Howard BA (2008) The role of NRG3 in mammary development. J Mammary Gland Biol Neoplasia 13(2):195-203
35. Gizatullin RZ, Muravenko OV, Al-Amin AN, Wang F., Protopopov AI, Kashuba VI, Zelenin AV, Zabarovsky E.R. (2000) Human NRG3 gene Map position 10q22-q23. Chromosome Res 8(6):560
36. Britsch S (2007) The neuregulin-I/ErbB signaling system in development and disease. Adv Anat Embryol Cell Biol 190:1-65
37. Yarden Y, Sliwkowski M.X. (2001) Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2(2):127-137
38. Zhang D, Sliwkowski MX, Mark M, Frantz G., Akita R, Sun Y, Hillan K., Crowley C, Brush J, Godowski PJ (1997) Neuregulin-3 (NRG3): a novel neural tissue-enriched protein that binds and activates ErbB4. Proc Natl Acad Sci U S A 94(18):9562-9567
39. Tang CS, Cheng G, So M.T., Yip BH, Miao XP, Wong EH, Ngan E.S., Lui VC, Song YQ, Chan D, Cheung K, Yuan ZW, Lei L, Chung PH, Liu XL, Wong KK, Marshall CR, Scherer SW, Cherny SS, Sham PC, Tam PK, Garcia-Barcelo MM (2012) Genome-wide copy number analysis uncovers a new HSCR gene: NRG3. PLoS Genet 8(5):e1002687
40. Erlich Y, Edvardson S, Hodges E., Zenvirt S, Thekkat P, Shaag A., Dor T, Hannon GJ, Elpeleg O (2011) Exome sequencing and disease-network analysis of a single family implicate a mutation in KIF1A in hereditary spastic paraparesis. Genome Res 21(5):658-664