Random mutagenesis of the mouse genome: A strategy for discovering gene function and the molecular basis of disease

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 300, Issue 1, 2011, Pages

  Nguyen, Nhung ^a   Judd, Louise M ^b   Kalantzis, Anastasia ^b   Whittle, Belinda ^c   Giraud, Andrew S ^b   Van Driel, Ian R ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^c Biology and Environment   (Australia)

Author keywords

Inflammatory bowel disease; Mouse models; N ethyl N nitrosourea; Phenotype driven

Indexed keywords

ANKYRIN; ETHYLNITROSOUREA; GENE PRODUCT; MUTAGENIC AGENT; NUCLEIC ACID; THROMBOPOIETIN; THROMBOPOIETIN RECEPTOR;

AMINO ACID SUBSTITUTION; CANCER RESEARCH; CARCINOGENESIS; CHRONIC INFLAMMATION; DNA ADDUCT; DNA POLYMORPHISM; ENTERITIS; FAMILIAL ADENOMATOUS POLYPOSIS; GENE FUNCTION; GENE IDENTIFICATION; GENE MAPPING; GENETIC DISORDER; GENETIC PREDISPOSITION; GENETIC SCREENING; GENETIC SUSCEPTIBILITY; GENOME; GENOTYPE PHENOTYPE CORRELATION; HERITABILITY; HUMAN; IMMUNE SYSTEM; INHERITANCE; KNOCKOUT MOUSE; LINKAGE ANALYSIS; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPE; POLYPOSIS; PRIORITY JOURNAL; REVIEW; THROMBOCYTOPENIA; WILD TYPE;

ANIMALS; BREEDING; DISEASE MODELS, ANIMAL; ETHYLNITROSOUREA; FEMALE; GENES; GENOME; GENOME-WIDE ASSOCIATION STUDY; INFLAMMATORY BOWEL DISEASES; MALE; MICE; MUTAGENESIS; PHENOTYPE;

EID: 78650772777     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00343.2010     Document Type: Review

References (77)

1. Abuin A, Hansen GM, Zambrowicz B. Gene trap mutagenesis. Handb Exp Pharmacol: 129-147, 2007.
2. Acevedo-Arozena A, Wells S, Potter P, Kelly M, Cox RD, Brown SD. ENU mutagenesis, a way forward to understand gene function. Annu Rev Genomics Hum Genet 9: 49-69, 2008.
3. Aigner B, Rathkolb B, Herbach N, Hrabe de Angelis M, Wanke R, Wolf E. Diabetes models by screen for hyperglycemia in phenotype-driven ENU mouse mutagenesis projects. Am J Physiol Endocrinol Metab 294: E232-E240, 2008. (Pubitemid 351231449)
4. Aigner B, Rathkolb B, Klempt M, Wagner S, Michel D, de Angelis MH, Wolf E. N-ethyl-N-nitrosourea mutagenesis produced a small number of mice with altered plasma electrolyte levels. J Biomed Sci 16: 53-59, 2009.
5. Augustin M, Sedlmeier R, Peters T, Huffstadt U, Kochmann E, Simon D, Schoniger M, Garke-Mayerthaler S, Laufs J, Mayhaus M, Franke S, Klose M, Graupner A, Kurzmann M, Zinser C, Wolf A, Voelkel M, Kellner M, Kilian M, Seelig S, Koppius A, Teubner A, Korthaus D, Nehls M, Wattler S. Efficient and fast targeted production of murine models based on ENU mutagenesis. Mamm Genome 16: 405-413, 2005. (Pubitemid 41557500)
6. Barbaric I, Wells S, Russ A, Dear TN. Spectrum of ENU-induced mutations in phenotype-driven and gene-driven screens in the mouse. Environ Mol Mutagen 48: 124-142, 2007. (Pubitemid 46365329)
7. Barnes MJ, Aksoylar H, Krebs P, Bourdeau T, Arnold CN, Xia Y, Khovananth K, Engel I, Sovath S, Lampe K, Laws E, Saunders A, Butcher GW, Kronenberg M, Steinbrecher K, Hildeman D, Grimes HL, Beutler B, Hoebe K. Loss of T cell and B cell quiescence precedes the onset of microbial flora-dependent wasting disease and intestinal inflammation in Gimap5-deficient mice. J Immunol 184: 3743-3754, 2010.
8. Brandl K, Rutschmann S, Li X, Du X, Xiao N, Schnabl B, Brenner DA, Beutler B. Enhanced sensitivity to DSS colitis caused by a hypomorphic Mbtps1 mutation disrupting the ATF6-driven unfolded protein response. Proc Natl Acad Sci USA 106: 3300-3305, 2009.
9. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77: 71-94, 1974.
10. Brown SD, Chambon P, de Angelis MH. EMPReSS: standardized phenotype screens for functional annotation of the mouse genome. Nat Genet 37: 1155, 2005. (Pubitemid 41568690)
11. Carpinelli MR, Hilton DJ, Metcalf D, Antonchuk JL, Hyland CD, Mifsud SL, Di Rago L, Hilton AA, Willson TA, Roberts AW, Ramsay RG, Nicola NA, Alexander WS. Suppressor screen in Mpl-/- mice: c-Myb mutation causes supraphysiological production of platelets in the absence of thrombopoietin signaling. Proc Natl Acad Sci USA 101: 6553-6558, 2004. (Pubitemid 38586012)
12. Chan ER, Lavender H, Li G, Haviernik P, Bunting KD, Adams MD. An ENU-induced recessive mutation in Mpl leads to thrombocytopenia with overdominance. Exp Hematol 37: 276-284, 2009.
13. Chen Y, Yee D, Dains K, Chatterjee A, Cavalcoli J, Schneider E, Om J, Woychik RP, Magnuson T. Genotype-based screen for ENU-induced mutations in mouse embryonic stem cells. Nat Genet 24: 314-317, 2000. (Pubitemid 30132206)
14. Cheng CH, Kikuchi T, Chen YH, Sabbagha NG, Lee YC, Pan HJ, Chang C, Chen YT. Mutations in the SLC2A10 gene cause arterial abnormalities in mice. Cardiovasc Res 81: 381-388, 2009.
15. Coghill EL, Hugill A, Parkinson N, Davison C, Glenister P, Clements S, Hunter J, Cox RD, Brown SD. A gene-driven approach to the identification of ENU mutants in the mouse. Nat Genet 30: 255-256, 2002.
16. Collins FS, Rossant J, Wurst W. A mouse for all reasons. Cell 128: 9-13, 2007.
17. Cook MC, Vinuesa CG, Goodnow CC. ENU-mutagenesis: insight into immune function and pathology. Curr Opin Immunol 18: 627-633, 2006.
18. Dokmanovic-Chouinard M, Chung WK, Chevre JC, Watson E, Yonan J, Wiegand B, Bromberg Y, Wakae N, Wright CV, Overton J, Ghosh S, Sathe GM, Ammala CE, Brown KK, Ito R, LeDuc C, Solomon K, Fischer SG, Leibel RL. Positional cloning of "Lisch-Like", a candidate modifier of susceptibility to type 2 diabetes in mice. PLoS Genet 4: e1000137, 2008.
19. Fernandez L, Marchuk DA, Moran JL, Beier DR, Rockman HA. An N-ethyl-N-nitrosourea mutagenesis recessive screen identifies two candidate regions for murine cardiomyopathy that map to chromosomes 1 and 15. Mamm Genome 20: 296-304, 2009.
20. Goldsworthy M, Hugill A, Freeman H, Horner E, Shimomura K, Bogani D, Pieles G, Mijat V, Arkell R, Bhattacharya S, Ashcroft FM, Cox RD. Role of the transcription factor sox4 in insulin secretion and impaired glucose tolerance. Diabetes 57: 2234-2244, 2008.
21. Hardisty-Hughes RE, Parker A, Brown SD. A hearing and vestibular phenotyping pipeline to identify mouse mutants with hearing impairment. Nat Protoc 5: 177-190, 2010.
22. Heazlewood CK, Cook MC, Eri R, Price GR, Tauro SB, Taupin D, Thornton DJ, Png CW, Crockford TL, Cornall RJ, Adams R, Kato M, Nelms KA, Hong NA, Florin TH, Goodnow CC, McGuckin MA. Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med 5: e54, 2008. (Pubitemid 351471694)
23. Hirsh D, Vanderslice R. Temperature-sensitive developmental mutants of Caenorhabditis elegans. Dev Biol 49: 220-235, 1976.
24. Hitotsumachi S, Carpenter DA, Russell WL. Dose-repetition increases the mutagenic effectiveness of N-ethyl-N-nitrosourea in mouse spermatogonia. Proc Natl Acad Sci USA 82: 6619-6621, 1985. (Pubitemid 16228871)
25. Hoebe K, Beutler B. Forward genetic analysis of TLR-signaling pathways: an evaluation. Adv Drug Deliv Rev 60: 824-829, 2008.
26. Hrabe de Angelis MH, Flaswinkel H, Fuchs H, Rathkolb B, Soewarto D, Marschall S, Heffner S, Pargent W, Wuensch K, Jung M, Reis A, Richter T, Alessandrini F, Jakob T, Fuchs E, Kolb H, Kremmer E, Schaeble K, Rollinski B, Roscher A, Peters C, Meitinger T, Strom T, Steckler T, Holsboer F, Klopstock T, Gekeler F, Schindewolf C, Jung T, Avraham K, Behrendt H, Ring J, Zimmer A, Schughart K, Pfeffer K, Wolf E, Balling R. Genome-wide, large-scale production of mutant mice by ENU mutagenesis. Nat Genet 25: 444-447, 2000.
27. Inoue M, Sakuraba Y, Motegi H, Kubota N, Toki H, Matsui J, Toyoda Y, Miwa I, Terauchi Y, Kadowaki T, Shigeyama Y, Kasuga M, Adachi T, Fujimoto N, Matsumoto R, Tsuchihashi K, Kagami T, Inoue A, Kaneda H, Ishijima J, Masuya H, Suzuki T, Wakana S, Gondo Y, Minowa O, Shiroishi T, Noda T. A series of maturity onset diabetes of the young, type 2 (MODY2) mouse models generated by a large-scale ENU mutagenesis program. Hum Mol Genet 13: 1147-1157, 2004.
28. Justice MJ, Carpenter DA, Favor J, Neuhauser-Klaus A, Hrabe de Angelis M, Soewarto D, Moser A, Cordes S, Miller D, Chapman V, Weber JS, Rinchik EM, Hunsicker PR, Russell WL, Bode VC. Effects of ENU dosage on mouse strains. Mamm Genome 11: 484-488, 2000.
29. Justice MJ, Noveroske JK, Weber JS, Zheng B, Bradley A. Mouse ENU mutagenesis. Hum Mol Genet 8: 1955-1963, 1999.
30. Kakugawa K, Yasuda T, Miura I, Kobayashi A, Fukiage H, Satoh R, Matsuda M, Koseki H, Wakana S, Kawamoto H, Yoshida H. A novel gene essential for the development of single positive thymocytes. Mol Cell Biol 29: 5128-5135, 2009.
31. Kauppi M, Murphy JM, de Graaf CA, Hyland CD, Greig KT, Metcalf D, Hilton AA, Nicola NA, Kile BT, Hilton DJ, Alexander WS. Point mutation in the gene encoding p300 suppresses thrombocytopenia in Mpl-/- mice. Blood 112: 3148-3153, 2008.
32. Kile BT, Hentges KE, Clark AT, Nakamura H, Salinger AP, Liu B, Box N, Stockton DW, Johnson RL, Behringer RR, Bradley A, Justice MJ. Functional genetic analysis of mouse chromosome 11. Nature 425: 81-86, 2003.
33. Kim JK, Kim E, Baek IC, Kim BK, Cho AR, Kim TY, Song CW, Seong JK, Yoon JB, Stenn KS, Parimoo S, Yoon SK. Overexpression of Hr links excessive induction of Wnt signaling to Marie Unna hereditary hypotrichosis. Hum Mol Genet 19: 445-453, 2010.
34. Lambe T, Simpson RJ, Dawson S, Bouriez-Jones T, Crockford TL, Lepherd M, Latunde-Dada GO, Robinson H, Raja KB, Campagna DR, Villarreal G Jr, Ellory JC, Goodnow CC, Fleming MD, McKie AT, Cornall RJ. Identification of a Steap3 endosomal targeting motif essential for normal iron metabolism. Blood 113: 1805-1808, 2009.
35. Largaespada DA. Transposon mutagenesis in mice. Methods Mol Biol 530: 379-390, 2009.
36. Lee B, Kano K, Young J, John SW, Nishina PM, Naggert JK, Naito K. A novel ENU-induced mutation, peewee, causes dwarfism in the mouse. Mamm Genome 20: 404-413, 2009.
37. Linterman MA, Rigby RJ, Wong R, Silva D, Withers D, Anderson G, Verma NK, Brink R, Hutloff A, Goodnow CC, Vinuesa CG. Roquin differentiates the specialized functions of duplicated T cell costimulatory receptor genes CD28 and ICOS. Immunity 30: 228-241, 2009.
38. Lloyd DJ, Wheeler MC, Gekakis N. A point mutation in Sec61alpha1 leads to diabetes and hepatosteatosis in mice. Diabetes 59: 460-470, 2010.
39. Loftus EV Jr. Clinical epidemiology of inflammatory bowel disease: Incidence, prevalence, and environmental influences. Gastroenterology 126: 1504-1517, 2004.
40. Malik I, Turk J, Mancuso DJ, Montier L, Wohltmann M, Wozniak DF, Schmidt RE, Gross RW, Kotzbauer PT. Disrupted membrane homeostasis and accumulation of ubiquitinated proteins in a mouse model of infantile neuroaxonal dystrophy caused by PLA2G6 mutations. Am J Pathol 172: 406-416, 2008.
41. McCart AE, Vickaryous NK, Silver A. Apc mice: models, modifiers and mutants. Pathol Res Pract 204: 479-490, 2008.
42. Michaud EJ, Culiat CT, Klebig ML, Barker PE, Cain KT, Carpenter DJ, Easter LL, Foster CM, Gardner AW, Guo ZY, Houser KJ, Hughes LA, Kerley MK, Liu Z, Olszewski RE, Pinn I, Shaw GD, Shinpock SG, Wymore AM, Rinchik EM, Johnson DK. Efficient gene-driven germ-line point mutagenesis of C57BL/6J mice. BMC Genomics 6: 164-181, 2005.
43. Miller G, Neilan M, Chia R, Gheryani N, Holt N, Charbit A, Wells S, Tucci V, Lalanne Z, Denny P, Fisher EM, Cheeseman M, Askew GN, Dear TN. ENU mutagenesis reveals a novel phenotype of reduced limb strength in mice lacking fibrillin 2. PLoS One 5: e9137, 2010.
44. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 247: 322-324, 1990.
45. Munroe RJ, Bergstrom RA, Zheng QY, Libby B, Smith R, John SW, Schimenti KJ, Browning VL, Schimenti JC. Mouse mutants from chemically mutagenized embryonic stem cells. Nat Genet 24: 318-321, 2000.
46. Nolan PM, Peters J, Strivens M, Rogers D, Hagan J, Spurr N, Gray IC, Vizor L, Brooker D, Whitehill E, Washbourne R, Hough T, Greenaway S, Hewitt M, Liu X, McCormack S, Pickford K, Selley R, Wells C, Tymowska-Lalanne Z, Roby P, Glenister P, Thornton C, Thaung C, Stevenson JA, Arkell R, Mburu P, Hardisty R, Kiernan A, Erven A, Steel KP, Voegeling S, Guenet JL, Nickols C, Sadri R, Nasse M, Isaacs A, Davies K, Browne M, Fisher EM, Martin J, Rastan S, Brown SD, Hunter J. A systematic, genome-wide, phenotype-driven mutagenesis programme for gene function studies in the mouse. Nat Genet 25: 440-443, 2000.
47. Nolan PM, Peters J, Vizor L, Strivens M, Washbourne R, Hough T, Wells C, Glenister P, Thornton C, Martin J, Fisher E, Rogers D, Hagan J, Reavill C, Gray I, Wood J, Spurr N, Browne M, Rastan S, Hunter J, Brown SD. Implementation of a large-scale ENU mutagenesis program: towards increasing the mouse mutant resource. Mamm Genome 11: 500-506, 2000.
48. Noveroske JK, Weber JS, Justice MJ. The mutagenic action of N-ethyl-N-nitrosourea in the mouse. Mamm Genome 11: 478-483, 2000.
49. Nusslein-Volhard C, Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 287: 795-801, 1980.
50. Osborn O, Sanchez-Alavez M, Brownell SE, Ross B, Klaus J, Dubins J, Beutler B, Conti B, Bartfai T. Metabolic characterization of a mouse deficient in all known leptin receptor isoforms. Cell Mol Neurobiol 30: 23-33, 2010.
51. Ostertag EM, Madison BB, Kano H. Mutagenesis in rodents using the L1 retrotransposon. Genome Biol 8, Suppl 1: S16-S24, 2007.
52. Quwailid MM, Hugill A, Dear N, Vizor L, Wells S, Horner E, Fuller S, Weedon J, McMath H, Woodman P, Edwards D, Campbell D, Rodger S, Carey J, Roberts A, Glenister P, Lalanne Z, Parkinson N, Coghill EL, McKeone R, Cox S, Willan J, Greenfield A, Keays D, Brady S, Spurr N, Gray I, Hunter J, Brown SD, Cox RD. A gene-driven ENU-based approach to generating an allelic series in any gene. Mamm Genome 15: 585-591, 2004.
53. Ramanadham S, Yarasheski KE, Silva MJ, Wohltmann M, Novack DV, Christiansen B, Tu X, Zhang S, Lei X, Turk J. Age-related changes in bone morphology are accelerated in group VIA phospholipase A2 (iPLA2beta)-null mice. Am J Pathol 172: 868-881, 2008.
54. Rank G, Sutton R, Marshall V, Lundie RJ, Caddy J, Romeo T, Fernandez K, McCormack MP, Cooke BM, Foote SJ, Crabb BS, Curtis DJ, Hilton DJ, Kile BT, Jane SM. Novel roles for erythroid Ankyrin-1 revealed through an ENU-induced null mouse mutant. Blood 113: 3352-3362, 2009.
55. Rinchik EM, Carpenter DA, Selby PB. A strategy for fine-structure functional analysis of a 6- to 11-centimorgan region of mouse chromosome 7 by high-efficiency mutagenesis. Proc Natl Acad Sci USA 87: 896-900, 1990.
56. Rogers DC, Fisher EM, Brown SD, Peters J, Hunter AJ, Martin JE. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Genome 8: 711-713, 1997.
57. Russell WL, Kelly EM, Hunsicker PR, Bangham JW, Maddux SC, Phipps EL. Specific-locus test shows ethylnitrosourea to be the most potent mutagen in the mouse. Proc Natl Acad Sci USA 76: 5818-5819, 1979.
58. Sakuraba Y, Sezutsu H, Takahasi KR, Tsuchihashi K, Ichikawa R, Fujimoto N, Kaneko S, Nakai Y, Uchiyama M, Goda N, Motoi R, Ikeda A, Karashima Y, Inoue M, Kaneda H, Masuya H, Minowa O, Noguchi H, Toyoda A, Sakaki Y, Wakana S, Noda T, Shiroishi T, Gondo Y. Molecular characterization of ENU mouse mutagenesis and archives. Biochem Biophys Res Commun 336: 609-616, 2005.
59. Sato H, Suzuki T, Ikeda K, Masuya H, Sezutsu H, Kaneda H, Kobayashi K, Miura I, Kurihara Y, Yokokura S, Nishida K, Tamai M, Gondo Y, Noda T, Wakana S. A monogenic dominant mutation in Rom1 generated by N-ethyl-N-nitrosourea mutagenesis causes retinal degeneration in mice. Mol Vis 16: 378-391, 2010.
60. Shinzawa K, Sumi H, Ikawa M, Matsuoka Y, Okabe M, Sakoda S, Tsujimoto Y. Neuroaxonal dystrophy caused by group VIA phospho-lipase A2 deficiency in mice: a model of human neurodegenerative disease. J Neurosci 28: 2212-2220, 2008.
61. Speca DJ, Rabbee N, Chihara D, Speed TP, Peterson AS. A genetic screen for behavioral mutations that perturb dopaminergic homeostasis in mice. Genes Brain Behav 5: 19-28, 2006.
62. Stylianou IM, Svenson KL, VanOrman SK, Langle Y, Millar JS, Paigen B, Rader DJ. Novel ENU-induced point mutation in scavenger receptor class B, member 1, results in liver specific loss of SCARB1 protein. PLoS One 4: e6521, 2009.
63. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C, Gould KA, Dove WF. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 256: 668-670, 1992.
64. Sundberg JP, Sundberg BA, Schofield P. Integrating mouse anatomy and pathology ontologies into a phenotyping database: tools for data capture and training. Mamm Genome 19: 413-419, 2008.
65. Takahasi KR, Sakuraba Y, Gondo Y. Mutational pattern and frequency of induced nucleotide changes in mouse ENU mutagenesis. BMC Mol Biol 8: 52-61, 2007.
66. Theodoratos A, Whittle B, Enders A, Tscharke DC, Roots CM, Goodnow CC, Fahrer AM. Mouse strains with point mutations in TAP1 and TAP2. Immunol Cell Biol 88: 72-78, 2010.
67. Toye AA, Moir L, Hugill A, Bentley L, Quarterman J, Mijat V, Hough T, Goldsworthy M, Haynes A, Hunter AJ, Browne M, Spurr N, Cox RD. A new mouse model of type 2 diabetes, produced by N-ethyl-nitrosourea mutagenesis, is the result of a missense mutation in the glucokinase gene. Diabetes 53: 1577-1583, 2004.
68. Van Burck L, Blutke A, Kautz S, Rathkolb B, Klaften M, Wagner S, Kemter E, Hrabe de Angelis M, Wolf E, Aigner B, Wanke R, Herbach N. Phenotypic and pathomorphological characteristics of a novel mutant mouse model for maturity-onset diabetes of the young type 2 (MODY 2). Am J Physiol Endocrinol Metab 298: E512-E523, 2010.
69. Vinuesa CG, Cook MC, Angelucci C, Athanasopoulos V, Rui L, Hill KM, Yu D, Domaschenz H, Whittle B, Lambe T, Roberts IS, Copley RR, Bell JI, Cornall RJ, Goodnow CC. A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity. Nature 435: 452-458, 2005.
70. Wada H, Yasuda T, Miura I, Watabe K, Sawa C, Kamijuku H, Kojo S, Taniguchi M, Nishino I, Wakana S, Yoshida H, Seino K. Establishment of an improved mouse model for infantile neuroaxonal dystrophy that shows early disease onset and bears a point mutation in Pla2g6. Am J Pathol 175: 2257-2263, 2009.
71. Westbrook AM, Szakmary A, Schiestl RH. Mechanisms of intestinal inflammation and development of associated cancers: lessons learned from mouse models. Mutat Res 705: 40-59, 2010.
72. Wilson L, Ching YH, Farias M, Hartford SA, Howell G, Shao H, Bucan M, Schimenti JC. Random mutagenesis of proximal mouse chromosome 5 uncovers predominantly embryonic lethal mutations. Genome Res 15: 1095-1105, 2005.
73. Wiltshire T, Pletcher MT, Batalov S, Barnes SW, Tarantino LM, Cooke MP, Wu H, Smylie K, Santrosyan A, Copeland NG, Jenkins NA, Kalush F, Mural RJ, Glynne RJ, Kay SA, Adams MD, Fletcher CF. Genome-wide single-nucleotide polymorphism analysis defines haplotype patterns in mouse. Proc Natl Acad Sci USA 100: 3380-3385, 2003.
74. Wong F, Fan L, Wells S, Hartley R, Mackenzie FE, Oyebode O, Brown R, Thomson D, Coleman MP, Blanco G, Ribchester RR. Axonal and neuromuscular synaptic phenotypes in Wld(S), SOD1(G93A) and ostes mutant mice identified by fiber-optic confocal microendoscopy. Mol Cell Neurosci 42: 296-307, 2009.
75. Yoshida Y, Makita Y, Heida N, Asano S, Matsushima A, Ishii M, Mochizuki Y, Masuya H, Wakana S, Kobayashi N, Toyoda T. PosMed (Positional Medline): prioritizing genes with an artificial neural network comprising medical documents to accelerate positional cloning. Nucleic Acids Res 37: W147-W152, 2009.
76. Yu D, Tan AH, Hu X, Athanasopoulos V, Simpson N, Silva DG, Hutloff A, Giles KM, Leedman PJ, Lam KP, Goodnow CC, Vinuesa CG. Roquin represses autoimmunity by limiting inducible T-cell costimulator messenger RNA. Nature 450: 299-303, 2007. (Pubitemid 350100535)
77. Zhang Z, Alpert D, Francis R, Chatterjee B, Yu Q, Tansey T, Sabol SL, Cui C, Bai Y, Koriabine M, Yoshinaga Y, Cheng JF, Chen F, Martin J, Schackwitz W, Gunn TM, Kramer KL, De Jong PJ, Pennacchio LA, Lo CW. Massively parallel sequencing identifies the gene Megf8 with ENU-induced mutation causing heterotaxy. Proc Natl Acad Sci USA 106: 3219-3224, 2009.