Large-scale mouse knockouts and phenotypes

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 4, Issue 6, 2012, Pages 547-563

  Ramírez Solis, Ramiro ^a   Ryder, Edward ^a   Houghton, Richard ^a   White, Jacqueline K ^a   Bottomley, Joanna ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPSY; BEHAVIORAL SCIENCE; CHIMERA; EMBRYONIC STEM CELL; ENERGY METABOLISM; GENE SILENCING; GENE TARGETING; KNOCKOUT GENE; KNOCKOUT MOUSE; NOCICEPTION; NONHUMAN; ORGAN SYSTEMS; PHENOTYPE; PROGENY; REVIEW;

ANIMALS; BEHAVIOR, ANIMAL; CARDIOVASCULAR SYSTEM; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; GENOME; IMMUNE SYSTEM; MICE; MICE, KNOCKOUT; MUSCULOSKELETAL SYSTEM; PHENOTYPE; SENSE ORGANS;

EID: 84867616638     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.1183     Document Type: Review

References (124)

1. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, et al. Initial sequencing and comparative analysis of the mouse genome. Nature 2002, 420:520-562.
2. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
3. Zambrowicz BP, Turner CA, Sands AT. Predicting drug efficacy: knockouts model pipeline drugs of the pharmaceutical industry. Curr Opin Pharmacol 2003, 3:563-570.
4. Zambrowicz BP, Sands AT. Knockouts model the 100 best-selling drugs-will they model the next 100? Nat Rev Drug Discov 2003, 2:38-51.
5. Bradley A, Evans M, Kaufman MH, Robertson E. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 1984, 309: 255-256.
6. Capecchi MR. The new mouse genetics: altering the genome by gene targeting. Trends Genet 1989, 5: 570-576.
7. Thomas KR, Capecchi MR. Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 1987, 51:503-512.
8. Doetschman T, Gregg RG, Maeda N, Hooper ML, Melton DW, Thompson S, Smithies O. Targetted correction of a mutant HPRT gene in mouse embryonic stem cells. Nature 1987, 330:576-578.
9. Ramirez-Solis R, Liu P, Bradley A. Chromosome engineering in mice. Nature 1995, 378:720-724.
10. Hasty P, Ramirez-Solis R, Krumlauf R, Bradley A. Introduction of a subtle mutation into the Hox-2.6 locus in embryonic stem cells. Nature 1991, 350: 243-246.
11. Biddinger SB, Kahn CR. From mice to men: insights into the insulin resistance syndromes. Annu Rev Physiol 2006, 68:123-158.
12. Stryke D, Kawamoto M, Huang CC, Johns SJ, King LA, Harper CA, Meng EC, Lee RE, Yee A, L'Italien L, et al. BayGenomics: a resource of insertional mutations in mouse embryonic stem cells. Nucleic Acids Res 2003, 31:278-281.
13. Osoegawa K, Tateno M, Woon PY, Frengen E, Mammoser AG, Catanese JJ, Hayashizaki Y, de Jong PJ. Bacterial artificial chromosome libraries for mouse sequencing and functional analysis. Genome Res 2000, 10:116-128.
14. Adams DJ, Quail MA, Cox T, van der Weyden L, Gorick BD, Su Q, Chan WI, Davies R, Bonfield JK, Law F, et al. A genome-wide, end-sequenced 129Sv BAC library resource for targeting vector construction. Genomics 2005, 86:753-758.
15. Adams DJ, Biggs PJ, Cox T, Davies R, van der Weyden L, Jonkers J, Smith J, Plumb B, Taylor R, Nishijima I, et al. Mutagenic insertion and chromosome engineering resource (MICER). Nat Genet 2004, 36:867-871.
16. Austin CP, Battey JF, Bradley A, Bucan M, Capecchi M, Collins FS, Dove WF, Duyk G, Dymecki S, Eppig JT, et al. The knockout mouse project. Nat Genet 2004, 36:921-924.
17. Auwerx J, Avner P, Baldock R, Ballabio A, Balling R, Barbacid M, Berns A, Bradley A, Brown S, Carmeliet P, et al. The European dimension for the mouse genome mutagenesis program. Nat Genet 2004, 36:925-927.
18. Collins FS, Rossant J, Wurst W. A mouse for all reasons. Cell 2007, 128:9-13.
19. Friedel RH, Seisenberger C, Kaloff C, Wurst W. EUCOMM-the European Conditional Mouse Mutagenesis Program. Brief Funct Genomic Proteomic 2007, 6:180-185.
20. Fuchs H, Gailus-Durner V, Adler T, Aguilar-Pimentel JA, Becker L, Calzada-Wack J, Da Silva-Buttkus P, Neff F, Gotz A, Hans W, et al. Mouse phenotyping. Methods 2011, 53:120-135.
21. Gailus-Durner V, Fuchs H, Adler T, Aguilar Pimentel A, Becker L, Bolle I, Calzada-Wack J, Dalke C, Ehrhardt N, Ferwagner B, et al. Systemic first-line phenotyping. Methods Mol Biol 2009, 530:463-509.
22. Fuchs H, Gailus-Durner V, Adler T, Pimentel JA, Becker L, Bolle I, Brielmeier M, Calzada-Wack J, Dalke C, Ehrhardt N, et al. The German Mouse Clinic: a platform for systemic phenotype analysis of mouse models. Curr Pharm Biotechnol 2009, 10:236-243.
23. Gailus-Durner V, Fuchs H, Becker L, Bolle I, Brielmeier M, Calzada-Wack J, Elvert R, Ehrhardt N, Dalke C, Franz TJ, et al. Introducing the German Mouse Clinic: open access platform for standardized phenotyping. Nat Methods 2005, 2:403-404.
24. Nolan PM, Peters J, Vizor L, Strivens M, Washbourne R, Hough T, Wells C, Glenister P, Thornton C, Martin J, et al. Implementation of a large-scale ENU mutagenesis program: towards increasing the mouse mutant resource. Mamm Genome 2000, 11:500-506.
25. Nolan PM, Peters J, Strivens M, Rogers D, Hagan J, Spurr N, Gray IC, Vizor L, Brooker D, Whitehill E, et al. A systematic, genome-wide, phenotype-driven mutagenesis programme for gene function studies in the mouse. Nat Genet 2000, 25:440-443.
26. Wakana S, Suzuki T, Furuse T, Kobayashi K, Miura I, Kaneda H, Yamada I, Motegi H, Toki H, Inoue M, et al. Introduction to the Japan Mouse Clinic at the RIKEN BioResource Center. Exp Anim 2009, 58: 443-450.
27. Justice MJ. Removing the cloak of invisibility: phenotyping the mouse. Dis Model Mech 2008, 1:109-112.
28. Clark AT, Goldowitz D, Takahashi JS, Vitaterna MH, Siepka SM, Peters LL, Frankel WN, Carlson GA, Rossant J, Nadeau JH, et al. Implementing large-scale ENU mutagenesis screens in North America. Genetica 2004, 122:51-64.
29. Solberg LC, Valdar W, Gauguier D, Nunez G, Taylor A, Burnett S, Arboledas-Hita C, Hernandez-Pliego P, Davidson S, Burns P, et al. A protocol for high-throughput phenotyping, suitable for quantitative trait analysis in mice. Mamm Genome 2006, 17:129-146.
30. Guan C, Ye C, Yang X, Gao J. A review of current large-scale mouse knockout efforts. Genesis 2010, 48: 73-85.
31. Schnutgen F, De-Zolt S, Van Sloun P, Hollatz M, Floss T, Hansen J, Altschmied J, Seisenberger C, Ghyselinck NB, Ruiz P, et al. Genomewide production of multipurpose alleles for the functional analysis of the mouse genome. Proc Natl Acad Sci U S A 2005, 102:7221-7226.
32. Zambrowicz BP, Abuin A, Ramirez-Solis R, Richter LJ, Piggott J, BeltrandelRio H, Buxton EC, Edwards J, Finch RA, Friddle CJ, et al. Wnk1 kinase deficiency lowers blood pressure in mice: a gene-trap screen to identify potential targets for therapeutic intervention. Proc Natl Acad Sci U S A 2003, 100:14109-14114.
33. Zambrowicz BP, Friedrich GA, Buxton EC, Lilleberg SL, Person C, Sands AT. Disruption and sequence identification of 2, 000 genes in mouse embryonic stem cells. Nature 1998, 392:608-611.
34. Skarnes WC, Moss JE, Hurtley SM, Beddington RS. Capturing genes encoding membrane and secreted proteins important for mouse development. Proc Natl Acad Sci U S A 1995, 92:6592-6596.
35. Carlson CM, Largaespada DA. Insertional mutagenesis in mice: new perspectives and tools. Nat Rev Genet. England: 2005, 6:568-580.
36. Testa G, Schaft J, van der Hoeven F, Glaser S, Anastassiadis K, Zhang Y, Hermann T, Stremmel W, Stewart AF. A reliable lacZ expression reporter cassette for multipurpose, knockout-first alleles. Genesis 2004, 38:151-158.
37. Nord AS, Chang PJ, Conklin BR, Cox AV, Harper CA, Hicks GG, Huang CC, Johns SJ, Kawamoto M, Liu S, et al. The International Gene Trap Consortium Website: a portal to all publicly available gene trap cell lines in mouse. Nucleic Acids Res 2006, 34 (Database issue):D642-D648.
38. Hansen GM, Markesich DC, Burnett MB, Zhu Q, Dionne KM, Richter LJ, Finnell RH, Sands AT, Zambrowicz BP, Abuin A. Large-scale gene trapping in C57BL/6N mouse embryonic stem cells. Genome Res 2008, 18:1670-1679.
39. Collins FS, Finnell RH, Rossant J, Wurst W. A new partner for the international knockout mouse consortium. Cell 2007, 129:235.
40. Valenzuela DM, Murphy AJ, Frendewey D, Gale NW, Economides AN, Auerbach W, Poueymirou WT, Adams NC, Rojas J, Yasenchak J, et al. High-throughput engineering of the mouse genome coupled with high-resolution expression analysis. Nat Biotechnol 2003, 21: 652-659.
41. Chan W, Costantino N, Li R, Lee SC, Su Q, Melvin D, Court DL, Liu P. A recombineering based approach for high-throughput conditional knockout targeting vector construction. Nucleic Acids Res 2007, 35:e64.
42. Liu P, Jenkins NA, Copeland NG. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 2003, 13: 476-484.
43. Fu J, Teucher M, Anastassiadis K, Skarnes W, Stewart AF. A recombineering pipeline to make conditional targeting constructs. Methods Enzymol 2010, 477: 125-144.
44. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, Mujica AO, Thomas M, Harrow J, Cox T, et al. A conditional knockout resource for the genome-wide study of mouse gene function. Nature 2011, 474:337-342.
45. Pettitt SJ, Liang Q, Rairdan XY, Moran JL, Prosser HM, Beier DR, Lloyd KC, Bradley A, Skarnes WC. Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nat Methods 2009, 6: 493-495.
46. Baryshnikova A, Andrews B. Neighboring-gene effect: a genetic uncertainty principle. Nat Methods 2012, 9: 341-343.
47. Ben-Shitrit T, Yosef N, Shemesh K, Sharan R, Ruppin E, Kupiec M. Systematic identification of gene annotation errors in the widely used yeast mutation collections. Nat Methods 2012, 9:373-378.
48. Kuhnert F, Mancuso MR, Hampton J, Stankunas K, Asano T, Chen CZ, Kuo CJ. Attribution of vascular phenotypes of the murine Egfl7 locus to the microRNA miR-126. Development 2008, 135:3989-3993.
49. Prosser HM, Koike-Yusa H, Cooper JD, Law FC, Bradley A. A resource of vectors and ES cells for targeted deletion of microRNAs in mice. Nat Biotechnol 2011, 29:840-845.
50. Cox BJ, Vollmer M, Tamplin O, Lu M, Biechele S, Gertsenstein M, van Campenhout C, Floss T, Kuhn R, Wurst W, et al. Phenotypic annotation of the mouse X chromosome. Genome Res 2010, 20:1154-1164.
51. Nuka S, Zhou W, Henry SP, Gendron CM, Schultz JB, Shinomura T, Johnson J, Wang Y, Keene DR, Ramirez-Solis R, et al. Phenotypic characterization of epiphycan-deficient and epiphycan/biglycan double-deficient mice. Osteoarthritis Cartilage 2010, 18:88-96.
52. Horan GS, Ramirez-Solis R, Featherstone MS, Wolgemuth DJ, Bradley A, Behringer RR. Compound mutants for the paralogous hoxa-4, hoxb-4, and hoxd-4 genes show more complete homeotic transformations and a dose-dependent increase in the number of vertebrae transformed. Genes Dev 1995, 9:1667-1677.
53. Ramirez-Solis R, Zheng H, Whiting J, Krumlauf R, Bradley A. Hoxb-4 (Hox-2.6) mutant mice show homeotic transformation of a cervical vertebra and defects in the closure of the sternal rudiments. Cell 1993, 73:279-294.
54. DeChiara TM, Poueymirou WT, Auerbach W, Frendewey D, Yancopoulos GD, Valenzuela DM. Producing fully ES cell-derived mice from eight-cell stage embryo injections. Methods Enzymol 2010, 476: 285-294.
55. Dechiara TM, Poueymirou WT, Auerbach W, Frendewey D, Yancopoulos GD, Valenzuela DM. VelociMouse: fully ES cell-derived F0-generation mice obtained from the injection of ES cells into eight-cell-stage embryos. Methods Mol Biol 2009, 530: 311-324.
56. Poueymirou WT, Auerbach W, Frendewey D, Hickey JF, Escaravage JM, Esau L, Dore AT, Stevens S, Adams NC, Dominguez MG, et al. F0 generation mice fully derived from gene-targeted embryonic stem cells allowing immediate phenotypic analyses. Nat Biotechnol 2007, 25:91-99.
57. Liu L, Nutter LM, Law N, McKerlie C. Sperm freezing and in vitro fertilization in three substrains of C57BL/6 mice. J Am Assoc Lab Anim Sci 2009, 48:39-43.
58. Ostermeier GC, Wiles MV, Farley JS, Taft RA. Conserving, distributing and managing genetically modified mouse lines by sperm cryopreservation. PLoS One 2008, 3:e2792.
59. Takeo T, Nakagata N. Reduced glutathione enhances fertility of frozen/thawed C57BL/6 mouse sperm after exposure to methyl-β-cyclodextrin. Biol Reprod 2011, 85:1066-1072.
60. Takeo T, Nakagata N. Combination medium of cryoprotective agents containing L-glutamine and methyl-{β}-cyclodextrin in a preincubation medium yields a high fertilization rate for cryopreserved C57BL/6J mouse sperm. Lab Anim 2010, 44:132-137.
61. Takeo T, Hoshii T, Kondo Y, Toyodome H, Arima H, Yamamura K, Irie T, Nakagata N. Methyl-β-cyclodextrin improves fertilizing ability of C57BL/6 mouse sperm after freezing and thawing by facilitating cholesterol efflux from the cells. Biol Reprod 2008, 78:546-551.
62. Bath ML. Optimized cryopreservation of mouse sperm based on fertilization rate. J Reprod Dev 2011, 57: 92-98.
63. Bath ML. Inhibition of in vitro fertilizing capacity of cryopreserved mouse sperm by factors released by damaged sperm, and stimulation by glutathione. PLoS One 2010, 5:e9387.
64. Bath ML. Simple and efficient in vitro fertilization with cryopreserved C57BL/6J mouse sperm. Biol Reprod 2003, 68:19-23.
65. Wilkinson P, Sengerova J, Matteoni R, Chen CK, Soulat G, Ureta-Vidal A, Fessele S, Hagn M, Massimi M, Pickford K, et al. EMMA-mouse mutant resources for the international scientific community. Nucleic Acids Res 2010, 38 (Database issue):D570-D576.
66. Lloyd KC. A knockout mouse resource for the biomedical research community. Ann N Y Acad Sci 2011, 1245:24-26.
67. Blanco S, Kurowski A, Nichols J, Watt FM, Benitah SA, Frye M. The RNA-methyltransferase Misu (NSun2) poises epidermal stem cells to differentiate. PLoS Genet 2011, 7:e1002403.
68. Crossan GP, van der Weyden L, Rosado IV, Langevin F, Gaillard PH, McIntyre RE, Gallagher F, Kettunen MI, Lewis DY, Brindle K, et al. Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat Genet 2011, 43:147-152.
69. Nijnik A, Clare S, Hale C, Raisen C, McIntyre RE, Yusa K, Everitt AR, Mottram L, Podrini C, Lucas M, et al. The critical role of histone H2A-deubiquitinase Mysm1 in hematopoiesis and lymphocyte differentiation. Blood 2012, 119:1370-1379.
70. Hopkins AL, Groom CR. The druggable genome. Nat Rev Drug Discov 2002, 1:727-730.
71. Beltrandelrio H, Kern F, Lanthorn T, Oravecz T, Piggott J, Powell D, Ramírez-Solis R, Sands AT, Zambrowicz B. Saturation screening of the druggable mammalian genome. In: Carroll PM, Fitzgerald K, eds. Model Organisms in Drug Discovery. Chichester, England: John Wiley & Sons, Ltd; 2003, 251-278.
72. Tang T, Li L, Tang J, Li Y, Lin WY, Martin F, Grant D, Solloway M, Parker L, Ye W, et al. A mouse knockout library for secreted and transmembrane proteins. Nat Biotechnol 2010, 28:749-755.
73. Brown SD, Chambon P, de Angelis MH. EMPReSS: standardized phenotype screens for functional annotation of the mouse genome. Nat Genet 2005, 37:1155.
74. Gates H, Mallon AM, Brown SD. High-throughput mouse phenotyping. Methods 2011, 53:394-404.
75. Morgan H, Beck T, Blake A, Gates H, Adams N, Debouzy G, Leblanc S, Lengger C, Maier H, Melvin D, et al. EuroPhenome: a repository for high-throughput mouse phenotyping data. Nucleic Acids Res 2010, 38 (Database issue):D577-D585.
76. Karp NA, Baker LA, Gerdin AK, Adams NC, Ramirez-Solis R, White JK. Optimising experimental design for high-throughput phenotyping in mice: a case study. Mamm Genome 2010, 21:467-476.
77. Meyer CW, Elvert R, Scherag A, Ehrhardt N, Gailus-Durner V, Fuchs H, Schafer H, Hrabe de Angelis M, Heldmaier G, Klingenspor M. Power matters in closing the phenotyping gap. Naturwissenschaften 2007, 94:401-406.
78. Bolon B. Whole mount enzyme histochemistry as a rapid screen at necropsy for expression of β-galactosidase (LacZ)-bearing transgenes: considerations for separating specific LacZ activity from nonspecific (endogenous) galactosidase activity. Toxicol Pathol 2008, 36:265-276.
79. Masuya H, Inoue M, Wada Y, Shimizu A, Nagano J, Kawai A, Inoue A, Kagami T, Hirayama T, Yamaga A, et al. Implementation of the modified-SHIRPA protocol for screening of dominant phenotypes in a large-scale ENU mutagenesis program. Mamm Genome 2005, 16:829-837.
80. 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 1997, 8:711-713.
81. Pieles G, Geyer SH, Szumska D, Schneider J, Neubauer S, Clarke K, Dorfmeister K, Franklyn A, Brown SD, Bhattacharya S, et al. microMRI-HREM pipeline for high-throughput, high-resolution phenotyping of murine embryos. J Anat 2007, 211:132-137.
82. Wahlsten D, Metten P, Phillips TJ, Boehm SL, 2nd, Burkhart-Kasch S, Dorow J, Doerksen S, Downing C, Fogarty J, Rodd-Henricks K, et al. Different data from different labs: lessons from studies of gene-environment interaction. J Neurobiol 2003, 54:283-311.
83. Wahlsten D. Standardizing tests of mouse behavior: reasons, recommendations, and reality. Physiol Behav 2001, 73:695-704.
84. Bryant CD, Zhang NN, Sokoloff G, Fanselow MS, Ennes HS, Palmer AA, McRoberts JA. Behavioral differences among C57BL/6 substrains: implications for transgenic and knockout studies. J Neurogenet 2008, 22:315-331.
85. Mackay TF, Anholt RR. Ain't misbehavin'? Genotype-environment interactions and the genetics of behavior. Trends Genet 2007, 23:311-314.
86. Chesler EJ, Wilson SG, Lariviere WR, Rodriguez-Zas SL, Mogil JS. Identification and ranking of genetic and laboratory environment factors influencing a behavioral trait, thermal nociception, via computational analysis of a large data archive. Neurosci Biobehav Rev 2002, 26:907-923.
87. Chesler EJ, Wilson SG, Lariviere WR, Rodriguez-Zas SL, Mogil JS. Influences of laboratory environment on behavior. Nat Neurosci 2002, 5:1101-1102.
88. Deacon RM. Housing, husbandry and handling of rodents for behavioral experiments. Nat Protoc 2006, 1:936-946.
89. Mandillo S, Tucci V, Holter SM, Meziane H, Banchaabouchi MA, Kallnik M, Lad HV, Nolan PM, Ouagazzal AM, Coghill EL, et al. Reliability, robustness, and reproducibility in mouse behavioral phenotyping: a cross-laboratory study. Physiol Genomics 2008, 34: 243-255.
90. Popkin BM. Is the obesity epidemic a national security issue around the globe? Current Opin Endocrinol Diabetes Obes 2011, 18:328-331.
91. Wang Y, Beydoun MA, Liang L, Caballero B, Kumanyika SK. Will all Americans become overweight or obese? estimating the progression and cost of the US obesity epidemic. Obesity (Silver Spring) 2008, 16: 2323-2330.
92. James WP, Rigby N, Leach R. Obesity and the metabolic syndrome: the stress on society. Ann N Y Acad Sci 2006, 1083:1-10.
93. Brommage R, Desai U, Revelli JP, Donoviel DB, Fontenot GK, Dacosta CM, Smith DD, Kirkpatrick LL, Coker KJ, Donoviel MS, et al. High-throughput screening of mouse knockout lines identifies true lean and obese phenotypes. Obesity (Silver Spring) 2008, 16: 2362-2367.
94. Brommage R. Validation and calibration of DEXA body composition in mice. Am J Physiol Endocrinol Metab 2003, 285:E454-E459.
95. Arch JR, Hislop D, Wang SJ, Speakman JR. Some mathematical and technical issues in the measurement and interpretation of open-circuit indirect calorimetry in small animals. Int J Obes (Lond) 2006, 30:1322-1331.
96. Ayala JE, Samuel VT, Morton GJ, Obici S, Croniger CM, Shulman GI, Wasserman DH, McGuinness OP. Standard operating procedures for describing and performing metabolic tests of glucose homeostasis in mice. Dis Model Mech 2010, 3:525-534.
97. Mogil JS, Wilson SG, Bon K, Lee SE, Chung K, Raber P, Pieper JO, Hain HS, Belknap JK, Hubert L, et al. Heritability of nociception II. 'Types' of nociception revealed by genetic correlation analysis. Pain 1999, 80:83-93.
98. Mogil JS, Wilson SG, Bon K, Lee SE, Chung K, Raber P, Pieper JO, Hain HS, Belknap JK, Hubert L, et al. Heritability of nociception I: responses of 11 inbred mouse strains on 12 measures of nociception. Pain 1999, 80:67-82.
99. Burgess RW, Cox GA, Seburn KL. Neuromuscular disease models and analysis Methods Mol Biol 2010, 602:347-393.
100. Abramow-Newerly W, Lipina T, Abramow-Newerly M, Kim D, Bechard AR, Xie G, Clapcote SJ, Roder JC. Methods to rapidly and accurately screen a large number of ENU mutagenized mice for abnormal motor phenotypes. Amyotroph Lateral Scler 2006, 7:112-118.
101. Curzon P, Zhang M, Radek RJ, Fox GB. The Behavioral Assessment of Sensorimotor Processes in the Mouse: Acoustic Startle, Sensory Gating, Locomotor Activity, Rotarod, and Beam Walking. Methods Behav Anal Neurosci, 2nd ed., Boca Raton, FL; 2009. Available at: http://www.ncbi.nlm.nih.gov/books/NBK5236/.
102. Luong TN, Carlisle HJ, Southwell A, Patterson PH. Assessment of motor balance and coordination in mice using the balance beam. J Vis Exp 2011, 49:e2376. doi:10.3791/2376.
103. Bothe GW, Bolivar VJ, Vedder MJ, Geistfeld JG. Genetic and behavioral differences among five inbred mouse strains commonly used in the production of transgenic and knockout mice. Genes Brain Behav 2004, 3:149-157.
104. Chu V, Otero JM, Lopez O, Morgan JP, Amende I, Hampton TG. Method for non-invasively recording electrocardiograms in conscious mice. BMC Physiol 2001, 1:6.
105. Xing S, Tsaih SW, Yuan R, Svenson KL, Jorgenson LM, So M, Paigen BJ, Korstanje R. Genetic influence on electrocardiogram time intervals and heart rate in aging mice. Am J Physiol Heart Circ Physiol 2009, 296:H1907-H1913.
106. Shen Y, Leatherbury L, Rosenthal J, Yu Q, Pappas MA, Wessels A, Lucas J, Siegfried B, Chatterjee B, Svenson K, et al. Cardiovascular phenotyping of fetal mice by noninvasive high-frequency ultrasound facilitates recovery of ENU-induced mutations causing congenital cardiac and extracardiac defects. Physiol Genomics 2005, 24:23-36.
107. Yu Q, Shen Y, Chatterjee B, Siegfried BH, Leatherbury L, Rosenthal J, Lucas JF, Wessels A, Spurney CF, Wu YJ, et al. ENU induced mutations causing congenital cardiovascular anomalies. Development 2004, 131:6211-6223.
108. Greco A, Mancini M, Gargiulo S, Gramanzini M, Claudio PP, Brunetti A, Salvatore M. Ultrasound biomicroscopy in small animal research: applications in molecular and preclinical imaging. J Biomed Biotechnol 2012, 2012:519238.
109. Bamforth SD, Schneider JE, Bhattacharya S. High-throughput analysis of mouse embryos by magnetic resonance imaging. Cold Spring Harb Protoc 2012, 2012:93-101.
110. Schneider JE, Bamforth SD, Farthing CR, Clarke K, Neubauer S, Bhattacharya S. Rapid identification and 3D reconstruction of complex cardiac malformations in transgenic mouse embryos using fast gradient echo sequence magnetic resonance imaging. J Mol Cell Cardiol 2003, 35:217-222.
111. Degenhardt K, Wright AC, Horng D, Padmanabhan A, Epstein JA. Rapid 3D phenotyping of cardiovascular development in mouse embryos by micro-CT with iodine staining. Circ Cardiovasc Imaging 2010, 3:314-322.
112. Zhou X, Jen PH, Seburn KL, Frankel WN, Zheng QY. Auditory brainstem responses in 10 inbred strains of mice. Brain Res 2006, 1091:16-26.
113. Zheng QY, Johnson KR, Erway LC. Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses. Hear Res 1999, 130:94-107.
114. Willott JF. Overview of methods for assessing the mouse auditory system. Curr Protoc Neurosci 2006, Chapter 8:Unit8 21A.
115. Adams DJ, van der Weyden L, Gergely FV, Arends MJ, Ng BL, Tannahill D, Kanaar R, Markus A, Morris BJ, Bradley A. BRCTx is a novel, highly conserved RAD18-interacting protein. Mol Cell Biol 2005, 25:779-788.
116. Schofield PN, Vogel P, Gkoutos GV, Sundberg JP. Exploring the elephant: histopathology in high-throughput phenotyping of mutant mice. Dis Model Mech 2012, 5:19-25.
117. van der Weyden L, White JK, Adams DJ, Logan DW. The mouse genetics toolkit: revealing function and mechanism. Genome Biol 2011, 12:224.
118. Smith CL, Eppig JT. The mammalian phenotype ontology: enabling robust annotation and comparative analysis. Wiley Interdiscip Rev Syst Biol Med 2009, 1:390-399.
119. Hancock JM, Adams NC, Aidinis V, Blake A, Bogue M, Brown SD, Chesler EJ, Davidson D, Duran C, Eppig JT, et al. Mouse Phenotype Database Integration Consortium: integration [corrected] of mouse phenome data resources. Mamm Genome 2007, 18:157-163.
120. Smith CL, Goldsmith CA, Eppig JT. The Mammalian Phenotype Ontology as a tool for annotating, analyzing and comparing phenotypic information. Genome Biol 2005, 6:R7.
121. Robinson PN, Mundlos S. The human phenotype ontology. Clin Genet 2010, 77:525-534.
122. Schofield PN, Gkoutos GV, Gruenberger M, Sundberg JP, Hancock JM. Phenotype ontologies for mouse and man: bridging the semantic gap. Dis Model Mech 2010, 3:281-289.
123. Schofield PN, Sundberg JP, Hoehndorf R, Gkoutos GV. New approaches to the representation and analysis of phenotype knowledge in human diseases and their animal models. Brief Funct Genomics 2011, 10:258-265.
124. Brown SD, Moore MW. Towards an encyclopaedia of mammalian gene function: the International Mouse Phenotyping Consortium. Dis Model Mech 2012, 5:289-292.