MARRVEL: Integration of Human and Model Organism Genetic Resources to Facilitate Functional Annotation of the Human Genome

American Journal of Human Genetics

Volumn 100, Issue 6, 2017, Pages 843-853

  Wang, Julia ^a,b   Al Ouran, Rami ^b,c   Hu, Yanhui ^d   Kim, Seon Young ^b,c   Wan, Ying Wooi ^b,c   Wangler, Michael F ^a,b,c,f   Yamamoto, Shinya ^a,b,c,f   Chao, Hsiao Tuan ^b,c   Comjean, Aram ^d   Mohr, Stephanie E ^d   Adams, Christopher J ^f   Adams, David R ^f   Alejandro, Mercedes E ^f   Allard, Patrick ^f   Ashley, Euan A ^f   Azamian, Mashid S ^f   Bacino, Carlos A ^f   Balasubramanyam, Ashok ^f   Barseghyan, Hayk ^f   Beggs, Alan H ^f   Bellen, Hugo J ^a,b,c,e,f   Bernstein, Jonathan A ^f   Bican, Anna ^f   Bick, David P ^f   Birch, Camille L ^f   Boone, Braden E ^f   Briere, Lauren C ^f   Brown, Donna M ^f   Brush, Matthew ^f   Burke, Elizabeth A ^f   Burrage, Lindsay C ^f   Chao, Katherine R ^f   Clark, Gary D ^f   Cogan, Joy D ^f   Cooper, Cynthia M ^f   Craigen, William J ^f   Davids, Mariska ^f   Dayal, Jyoti G ^f   Dell'Angelica, Esteban C ^f   Dhar, Shweta U ^f   Dipple, Katrina M ^f   Donnell Fink, Laurel A ^f   Dorrani, Naghmeh ^f   Dorset, Daniel C ^f   Draper, David D ^f   Dries, Annika M ^f   Eckstein, David J ^f   Emrick, Lisa T ^f   Eng, Christine M ^f   Esteves, Cecilia ^f   Estwick, Tyra ^f   Fisher, Paul G ^f   Frisby, Trevor S ^f   Frost, Kate ^f   Gahl, William A ^f   Gartner, Valerie ^f   Godfrey, Rena A ^f   Goheen, Mitchell ^f   Golas, Gretchen A ^f   Goldstein, David B ^f   Gordon, Mary G ^f   Gould, Sarah E ^f   Gourdine, Jean Philippe F ^f   Graham, Brett H ^f   Groden, Catherine A ^f   Gropman, Andrea L ^f   Hackbarth, Mary E ^f   Haendel, Melissa ^f   Hamid, Rizwan ^f   Hanchard, Neil A ^f   Handley, Lori H ^f   Hardee, Isabel ^f   Herzog, Matthew R ^f   Holm, Ingrid A ^f   Howerton, Ellen M ^f   Jacob, Howard J ^f   Jain, Mahim ^f   Jiang, Yong hui ^f   Johnston, Jean M ^f   Jones, Angela L ^f   Koehler, Alanna E ^f   Koeller, David M ^f   Kohane, Isaac S ^f   Kohler, Jennefer N ^f   Krasnewich, Donna M ^f   Krieg, Elizabeth L ^f   Krier, Joel B ^f   Kyle, Jennifer E ^f   Lalani, Seema R ^f   Latham, Lea ^f   Latour, Yvonne L ^f   Lau, C Christopher ^f   Lazar, Jozef ^f   Lee, Brendan H ^f   Lee, Hane ^f   Lee, Paul R ^f   Levy, Shawn E ^f   Levy, Denise J ^f   Lewis, Richard A ^f   Liebendorfer, Adam P ^f   Lincoln, Sharyn A ^f   Loomis, Carson R ^f   Loscalzo, Joseph ^f   Maas, Richard L ^f   Macnamara, Ellen F ^f   MacRae, Calum A ^f   Maduro, Valerie V ^f   Malicdan, May Christine V ^f   Mamounas, Laura A ^f   Manolio, Teri A ^f   Markello, Thomas C ^f   Mazur, Paul ^f   McCarty, Alexandra J ^f   McConkie Rosell, Allyn ^f   McCray, Alexa T ^f   Metz, Thomas O ^f   Might, Matthew ^f   Moretti, Paolo M ^f   Mulvihill, John J ^f   Murphy, Jennifer L ^f   Muzny, Donna M ^f   Nehrebecky, Michele E ^f   Nelson, Stan F ^f   Newberry, J Scott ^f   Newman, John H ^f   Nicholas, Sarah K ^f   Novacic, Donna ^f   Orange, Jordan S ^f   Pallais, J Carl ^f   Palmer, Christina G S ^f   Papp, Jeanette C ^f   Pena, Loren D M ^f   Phillips, John A ^f   Posey, Jennifer E ^f   Postlethwait, John H ^f   Potocki, Lorraine ^f   Pusey, Barbara N ^f   Ramoni, Rachel B ^f   Robertson, Amy K ^f   Rodan, Lance H ^f   Rosenfeld, Jill A ^f   Sadozai, Sarah ^f   Schaffer, Katherine E ^f   Schoch, Kelly ^f   Schroeder, Molly C ^f   Scott, Daryl A ^f   Sharma, Prashant ^f   Shashi, Vandana ^f   Silverman, Edwin K ^f   Sinsheimer, Janet S ^f   Soldatos, Ariane G ^f   Spillmann, Rebecca C ^f   Splinter, Kimberly ^f   Stoler, Joan M ^f   Stong, Nicholas ^f   Strong, Kimberly A ^f   Sullivan, Jennifer A ^f   Sweetser, David A ^f   Thomas, Sara P ^f   Tifft, Cynthia J ^f   Tolman, Nathanial J ^f   Toro, Camilo ^f   Tran, Alyssa A ^f   Valivullah, Zaheer M ^f   Vilain, Eric ^f   Waggott, Daryl M ^f   Wahl, Colleen E ^f   Walley, Nicole M ^f   Walsh, Chris A ^f   Warburton, Mike ^f   Ward, Patricia A ^f   Waters, Katrina M ^f   Webb Robertson, Bobbie Jo M ^f   Weech, Alec A ^f   Westerfield, Monte ^f   Wheeler, Matthew T ^f   Wise, Anastasia L ^f   Wolfe, Lynne A ^f   Worthey, Elizabeth A ^f   Yang, Yaping ^f   Yu, Guoyun ^f   Zornio, Patricia A ^f   Perrimon, Norbert ^d   Liu, Zhandong ^b,c   more..

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b BCM   (United States)

^c TEXAS CHILDREN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f NONE

Author keywords

ClinVar; Diopt; ExAC; FlyBase; genetic diseases; Geno2MP; MGI; rare diseases; variants of unknown significance; Zfin

Indexed keywords

ARTICLE; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; GENETIC DATABASE; GENETIC RESOURCE; GENOME ANALYSIS; HUMAN; HUMAN GENOME; MUS MUSCULUS; NONHUMAN; PRIORITY JOURNAL; RATTUS NORVEGICUS; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SEQUENCE HOMOLOGY; GENETIC VARIATION; MOLECULAR GENETICS; SOFTWARE;

DATABASES, GENETIC; GENETIC VARIATION; GENOME, HUMAN; HUMANS; MOLECULAR SEQUENCE ANNOTATION; SOFTWARE;

EID: 85019064193     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2017.04.010     Document Type: Article

References (46)

1. 1 Richards, S., Aziz, N., Bale, S., Bick, D., Das, S., Gastier-Foster, J., Grody, W.W., Hegde, M., Lyon, E., Spector, E., et al., ACMG Laboratory Quality Assurance Committee. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet. Med. 17 (2015), 405–424.
2. 2 Bellen, H.J., Yamamoto, S., Morgan's legacy: fruit flies and the functional annotation of conserved genes. Cell 163 (2015), 12–14.
3. 3 Chong, J.X., Buckingham, K.J., Jhangiani, S.N., Boehm, C., Sobreira, N., Smith, J.D., Harrell, T.M., McMillin, M.J., Wiszniewski, W., Gambin, T., et al., Centers for Mendelian Genomics. The genetic basis of Mendelian phenotypes: discoveries, challenges, and opportunities. Am. J. Hum. Genet. 97 (2015), 199–215.
4. 4 Gahl, W.A., Mulvihill, J.J., Toro, C., Markello, T.C., Wise, A.L., Ramoni, R.B., Adams, D.R., Tifft, C.J., UDN. The NIH Undiagnosed Diseases Program and Network: applications to modern medicine. Mol. Genet. Metab. 117 (2016), 393–400.
5. 5 O'Roak, B.J., Deriziotis, P., Lee, C., Vives, L., Schwartz, J.J., Girirajan, S., Karakoc, E., Mackenzie, A.P., Ng, S.B., Baker, C., et al. Exome sequencing in sporadic autism spectrum disorders identifies severe de novo mutations. Nat. Genet. 43 (2011), 585–589.
6. 6 Wright, C.F., Fitzgerald, T.W., Jones, W.D., Clayton, S., McRae, J.F., van Kogelenberg, M., King, D.A., Ambridge, K., Barrett, D.M., Bayzetinova, T., et al., DDD study. Genetic diagnosis of developmental disorders in the DDD study: a scalable analysis of genome-wide research data. Lancet 385 (2015), 1305–1314.
7. 7 Ramocki, M.B., Zoghbi, H.Y., Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature 455 (2008), 912–918.
8. 8 Marygold, S.J., Crosby, M.A., Goodman, J.L., FlyBase Consortium. Using FlyBase, a database of Drosophila genes and genomes. Methods Mol. Biol. 1478 (2016), 1–31.
9. 9 Eppig, J.T., Smith, C.L., Blake, J.A., Ringwald, M., Kadin, J.A., Richardson, J.E., Bult, C.J., Mouse genome informatics (MGI): resources for mining mouse genetic, genomic, and biological data in support of primary and translational research. Methods Mol. Biol. 1488 (2017), 47–73.
10. 10 Ruzicka, L., Bradford, Y.M., Frazer, K., Howe, D.G., Paddock, H., Ramachandran, S., Singer, A., Toro, S., Van Slyke, C.E., Eagle, A.E., et al. ZFIN, the zebrafish model organism database: updates and new directions. Genesis 53 (2015), 498–509.
11. 11 Chao, H.-T., Davids, M., Burke, E., Pappas, J.G., Rosenfeld, J.A., McCarty, A.J., Davis, T., Wolfe, L., Toro, C., Tifft, C., et al. A syndromic neurodevelopmental disorder caused by de novo variants in EBF3. Am. J. Hum. Genet. 100 (2017), 128–137.
12. 12 Chen, K., Ho, T.S.-Y., Lin, G., Tan, K.L., Rasband, M.N., Bellen, H.J., Ackermann, E., Guo, S., Booten, S., Alvarado, L., et al. Loss of Frataxin activates the iron/sphingolipid/PDK1/Mef2 pathway in mammals. eLife 5 (2016), 43–44.
13. 13 Yoon, W.H., Sandoval, H., Nagarkar-Jaiswal, S., Jaiswal, M., Yamamoto, S., Haelterman, N.A., Putluri, N., Putluri, V., Sreekumar, A., Tos, T., et al. Loss of Nardilysin, a mitochondrial co-chaperone for α-Ketoglutarate Dehydrogenase, promotes mTORC1 activation and neurodegeneration. Neuron 93 (2017), 115–131.
14. 14 Amberger, J.S., Bocchini, C.A., Schiettecatte, F., Scott, A.F., Hamosh, A., OMIM.org: Online Mendelian Inheritance in Man (OMIM®), an online catalog of human genes and genetic disorders. Nucleic Acids Res. 43 (2015), D789–D798.
15. 15 Lek, M., Karczewski, K.J., Minikel, E.V., Samocha, K.E., Banks, E., Fennell, T., O'Donnell-Luria, A.H., Ware, J.S., Hill, A.J., Cummings, B.B., et al., Exome Aggregation Consortium. Analysis of protein-coding genetic variation in 60,706 humans. Nature 536 (2016), 285–291.
16. 16 Landrum, M.J., Lee, J.M., Benson, M., Brown, G., Chao, C., Chitipiralla, S., Gu, B., Hart, J., Hoffman, D., Hoover, J., et al. ClinVar: public archive of interpretations of clinically relevant variants. Nucleic Acids Res. 44:D1 (2016), D862–D868.
17. 17 MacDonald, J.R., Ziman, R., Yuen, R.K.C., Feuk, L., Scherer, S.W., The Database of Genomic Variants: a curated collection of structural variation in the human genome. Nucleic Acids Res. 42 (2014), D986–D992.
18. 18 Firth, H.V., Richards, S.M., Bevan, A.P., Clayton, S., Corpas, M., Rajan, D., Van Vooren, S., Moreau, Y., Pettett, R.M., Carter, N.P., DECIPHER: database of chromosomal imbalance and phenotype in humans using Ensembl resources. Am. J. Hum. Genet. 84 (2009), 524–533.
19. 19 Cherry, J.M., Hong, E.L., Amundsen, C., Balakrishnan, R., Binkley, G., Chan, E.T., Christie, K.R., Costanzo, M.C., Dwight, S.S., Engel, S.R., et al. Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res. 40 (2012), D700–D705.
20. 20 Wood, V., Harris, M.A., McDowall, M.D., Rutherford, K., Vaughan, B.W., Staines, D.M., Aslett, M., Lock, A., Bähler, J., Kersey, P.J., Oliver, S.G., PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res. 40 (2012), D695–D699.
21. 21 Howe, K.L., Bolt, B.J., Cain, S., Chan, J., Chen, W.J., Davis, P., Done, J., Down, T., Gao, S., Grove, C., et al. WormBase 2016: expanding to enable helminth genomic research. Nucleic Acids Res. 44:D1 (2016), D774–D780.
22. 22 Shimoyama, M., De Pons, J., Hayman, G.T., Laulederkind, S.J.F., Liu, W., Nigam, R., Petri, V., Smith, J.R., Tutaj, M., Wang, S.-J., et al. The Rat Genome Database 2015: genomic, phenotypic and environmental variations and disease. Nucleic Acids Res. 43 (2015), D743–D750.
23. 23 Yu, Y., Fuscoe, J.C., Zhao, C., Guo, C., Jia, M., Qing, T., Bannon, D.I., Lancashire, L., Bao, W., Du, T., et al. A rat RNA-seq transcriptomic BodyMap across 11 organs and 4 developmental stages. Nat. Commun., 5, 2014, 3230.
24. 24 Huntley, R.P., Sawford, T., Mutowo-Meullenet, P., Shypitsyna, A., Bonilla, C., Martin, M.J., O'Donovan, C., The GOA database: gene ontology annotation updates for 2015. Nucleic Acids Res. 43 (2015), D1057–D1063.
25. 25 Carithers, L.J., Ardlie, K., Barcus, M., Branton, P.A., Britton, A., Buia, S.A., Compton, C.C., DeLuca, D.S., Peter-Demchok, J., Gelfand, E.T., et al., GTEx Consortium. A novel approach to high-quality postmortem tissue procurement: the GTEx Project. Biopreserv. Biobank. 13 (2015), 311–319.
26. 26 Uhlén, M., Fagerberg, L., Hallström, B.M., Lindskog, C., Oksvold, P., Mardinoglu, A., Sivertsson, Å., Kampf, C., Sjöstedt, E., Asplund, A., et al. Proteomics. Tissue-based map of the human proteome. Science, 347, 2015, 1260419.
27. 27 Hu, Y., Flockhart, I., Vinayagam, A., Bergwitz, C., Berger, B., Perrimon, N., Mohr, S.E., McKusick, V., Hamosh, A., Scott, A., et al. An integrative approach to ortholog prediction for disease-focused and other functional studies. BMC Bioinformatics, 12, 2011, 357.
28. 28 Yates, B., Braschi, B., Gray, K.A., Seal, R.L., Tweedie, S., Bruford, E.A., Genenames.org: the HGNC and VGNC resources in 2017. Nucleic Acids Res. 45:D1 (2017), D619–D625.
29. 29 den Dunnen, J.T., Describing sequence variants using HGVS nomenclature. Methods Mol. Biol. 1492 (2017), 243–251.
30. 30 Wildeman, M., van Ophuizen, E., den Dunnen, J.T., Taschner, P.E.M., Improving sequence variant descriptions in mutation databases and literature using the Mutalyzer sequence variation nomenclature checker. Hum. Mutat. 29 (2008), 6–13.
31. 31 Axmark, D., and Widenius, M. (2002). MySQL Reference Manual, P. DuBois, ed. (O'Reilly & Assoc.).
32. 32 NCBI Resource Coordinators. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 44:D1 (2016), D7–D19.
33. 33 Gene Ontology Consortium. Gene Ontology Consortium: going forward. Nucleic Acids Res. 43 (2015), D1049–D1056.
34. 34 Karaca, E., Harel, T., Pehlivan, D., Jhangiani, S.N., Gambin, T., Coban Akdemir, Z., Gonzaga-Jauregui, C., Erdin, S., Bayram, Y., Campbell, I.M., et al. Genes that affect brain structure and function identified by rare variant analyses of Mendelian neurologic disease. Neuron 88 (2015), 499–513.
35. 35 Miosge, L.A., Field, M.A., Sontani, Y., Cho, V., Johnson, S., Palkova, A., Balakishnan, B., Liang, R., Zhang, Y., Lyon, S., et al. Comparison of predicted and actual consequences of missense mutations. Proc. Natl. Acad. Sci. USA 112 (2015), E5189–E5198.
36. 36 Adzhubei, I.A., Schmidt, S., Peshkin, L., Ramensky, V.E., Gerasimova, A., Bork, P., Kondrashov, A.S., Sunyaev, S.R., A method and server for predicting damaging missense mutations. Nat. Methods 7 (2010), 248–249.
37. 37 Katsonis, P., Koire, A., Wilson, S.J., Hsu, T.-K., Lua, R.C., Wilkins, A.D., Lichtarge, O., Single nucleotide variations: biological impact and theoretical interpretation. Protein Sci. 23 (2014), 1650–1666.
38. 38 Katsonis, P., Lichtarge, O., A formal perturbation equation between genotype and phenotype determines the evolutionary action of protein-coding variations on fitness. Genome Res. 24 (2014), 2050–2058.
39. 39 Sun, S., Yang, F., Tan, G., Costanzo, M., Oughtred, R., Hirschman, J., Theesfeld, C.L., Bansal, P., Sahni, N., Yi, S., et al. An extended set of yeast-based functional assays accurately identifies human disease mutations. Genome Res. 26 (2016), 670–680.
40. 40 Mungall, C.J., McMurry, J.A., Köhler, S., Balhoff, J.P., Borromeo, C., Brush, M., Carbon, S., Conlin, T., Dunn, N., Engelstad, M., et al. The Monarch Initiative: an integrative data and analytic platform connecting phenotypes to genotypes across species. Nucleic Acids Res. 45:D1 (2017), D712–D722.
41. 41 Robinson, P.N., Köhler, S., Oellrich, A., Wang, K., Mungall, C.J., Lewis, S.E., Washington, N., Bauer, S., Seelow, D., Krawitz, P., et al., Sanger Mouse Genetics Project. Improved exome prioritization of disease genes through cross-species phenotype comparison. Genome Res. 24 (2014), 340–348.
42. 42 Wang, K., Li, M., Hakonarson, H., ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res., 38, 2010, e164.
43. 43 Mungall, C., McMurry, J., Koehler, S., Balhoff, J., Borromeo, C., Brush, M., Carbon, S., Conlin, T., Dunn, N., Engelstad, M., et al. The Monarch Initiative: Insights across species reveal human disease mechanisms. bioRxiv, 2016, 10.1101/055756.
44. 44 McGary, K.L., Park, T.J., Woods, J.O., Cha, H.J., Wallingford, J.B., Marcotte, E.M., Systematic discovery of nonobvious human disease models through orthologous phenotypes. Proc. Natl. Acad. Sci. USA 107 (2010), 6544–6549.
45. 45 Kaiser, J., Lock, A., Harris, M.A., Nurse, P., Wood, V., Kaiser, J., Bond, M., Holthaus, S.-M., Tammen, I., Tear, G., et al. BIOMEDICAL RESOURCES. Funding for key data resources in jeopardy. Science, 351, 2016 14–14.
46. 46 Yang, Y., Muzny, D.M., Xia, F., Niu, Z., Person, R., Ding, Y., Ward, P., Braxton, A., Wang, M., Buhay, C., et al. Molecular findings among patients referred for clinical whole-exome sequencing. JAMA 312 (2014), 1870–1879.