A nonsense mutation in PLD4 is associated with a zinc deficiency-like syndrome in Fleckvieh cattle

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Jung, Simone ^a   Pausch, Hubert ^a   Langenmayer, Martin C ^b   Schwarzenbacher, Hermann ^c   Majzoub Altweck, Monir ^b   Gollnick, Nicole S ^b   Fries, Ruedi ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c ZucbtData EDV Dienstleistungen GmbH   (Austria)

Author keywords

Autozygosity mapping; Fleckvieh; Next generation sequencing; Nonsense mutation; PLD4; Recessive inheritance; Zinc deficiency like

Indexed keywords

GENOMIC DNA; PHOSPHOLIPASE D; PHOSPHOLIPASE D4; UNCLASSIFIED DRUG; ZINC; ZINC TRANSPORTER; LIM PROTEIN; STOP CODON;

ANIMAL TISSUE; ARTICLE; AUTOZYGOSITY; BOVINE HEREDITARY ZINC DEFICIENCY; CALF (BOVINE); CATTLE BREED; CHROMOSOME 21; CONTROLLED STUDY; CRIP1 GENE; CRIP2 GENE; FEMALE; FLECKVIEH CATTLE; GENE FREQUENCY; GENE MAPPING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOME SIZE; GENOTYPE; HOMOZYGOSITY; MALABSORPTION; MALE; NONHUMAN; NONSENSE MUTATION; PLD4 GENE; RECESSIVE INHERITANCE; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SKIN DEFECT; SURVIVAL RATE; ZINC DEFICIENCY; ZYGOSITY; ANIMAL; BOVINAE; CATTLE DISEASE; CHROMOSOME MAP; DERMIS; DISORDERS OF METAL METABOLISM; DNA SEQUENCE; GENETICS; HIGH THROUGHPUT SEQUENCING; HOMOZYGOTE; METABOLISM; PATHOLOGY; PHENOTYPE; STOP CODON; SYNDROME;

ANIMALIA; BOS; BOVINAE; FRIESIA;

ANIMALS; CATTLE; CATTLE DISEASES; CHROMOSOME MAPPING; CODON, NONSENSE; DERMIS; GENOTYPE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOMOZYGOTE; LIM DOMAIN PROTEINS; METAL METABOLISM, INBORN ERRORS; PHENOTYPE; PHOSPHOLIPASE D; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA; SYNDROME; ZINC;

EID: 84904524928     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-623     Document Type: Article

References (51)

1. Online Mendelian Inheritance in Animals, OMIA, Faculty of Veterinary Science, University of Sydney (January 2014). http://omia.angis.org.au/.
2. Van Vleck LD. Effect of artificial insemination on frequency of undesirable recessive genes. J Dairy Sci 1967, 50:201-204. 10.3168/jds.S0022-0302(67)87388-0, 6032169.
3. Charlier C, Coppieters W, Rollin F, Desmecht D, Agerholm JS, Cambisano N, Carta E, Dardano S, Dive M, Fasquelle C, Frennet J-C, Hanset R, Hubin X, Jorgensen C, Karim L, Kent M, Harvey K, Pearce BR, Simon P, Tama N, Nie H, Vandeputte S, Lien S, Longeri M, Fredholm M, Harvey RJ, Georges M. Highly effective SNP-based association mapping and management of recessive defects in livestock. Nat Genet 2008, 40:449-454. 10.1038/ng.96, 18344998.
4. Machen M, Montgomery T, Holland R, Braselton E, Dunstan R, Brewer G, Yuzbasiyan-Gurkan V. Bovine hereditary zinc deficiency: lethal trait A 46. J Vet Diagn Invest 1996, 8:219-227. 10.1177/104063879600800212, 8744744.
5. Brummerstedt E. Animal model of human disease: acrodermatitis enteropathica, zinc malabsorption. Am J Pathol 1977, 87:725-728. 2032138, 559415.
6. Stöber M. Parakeratosis in black pied calves: 1: clinical findings and etiology. DTW Dtsch Tierarztl Wochenschr 1971, 78:257-265.
7. Wang K, Zhou B, Kuo Y-M, Zemansky J, Gitschier J. A novel member of a zinc transporter family is defective in acrodermatitis enteropathica. Am J Hum Genet 2002, 71:66-73. 10.1086/341125, 419995, 12032886.
8. Yuzbasiyan-Gurkan V, Bartlett E. Identification of a unique splice site variant in SLC39A4 in bovine hereditary zinc deficiency, lethal trait A46: an animal model of acrodermatitis enteropathica. Genomics 2006, 88:521-526. 10.1016/j.ygeno.2006.03.018, 16714095.
9. Dufner-Beattie J, Weaver BP, Geiser J, Bilgen M, Larson M, Xu W, Andrews GK. The mouse acrodermatitis enteropathica gene Slc39a4 (Zip4) is essential for early development and heterozygosity causes hypersensitivity to zinc deficiency. Hum Mol Genet 2007, 16:1391-1399. 10.1093/hmg/ddm088, 17483098.
10. Florea L, Souvorov A, Kalbfleisch TS, Salzberg SL. Genome assembly has a major impact on gene content: a comparison of annotation in two bos taurus assemblies. PLoS One 2011, 6:e21400. 10.1371/journal.pone.0021400, 3120881, 21731731.
11. Hallquist NA, Khoo C, Cousins RJ. Lipopolysaccharide regulates cysteine-rich intestinal protein, a zinc-finger protein, in immune cells and plasma. J Leukoc Biol 1996, 59:172-177.
12. Hempe JM, Cousins RJ. Cysteine-rich intestinal protein binds zinc during transmucosal zinc transport. Proc Natl Acad Sci USA 1991, 88:9671-9674. 10.1073/pnas.88.21.9671, 52780, 1946385.
13. Cousins RJ, Lanningham-Foster L. Regulation of cysteine-rich intestinal protein, a zinc finger protein, by mediators of the immune response. J Infect Dis 2000, 182(Suppl 1):S81-84.
14. Jansen S, Aigner B, Pausch H, Wysocki M, Eck S, Benet-Pagès A, Graf E, Wieland T, Strom TM, Meitinger T, Fries R. Assessment of the genomic variation in a cattle population by re-sequencing of key animals at low to medium coverage. BMC Genomics 2013, 14:446. 10.1186/1471-2164-14-446, 3716689, 23826801.
15. Daetwyler HD, Capitan A, Pausch H, Stothard P, van Binsbergen R, Brøndum RF, Liao X, Djari A, Rodriguez SC, Grohs C, Esquerré D, Bouchez O, Rossignol M-N, Klopp C, Rocha D, Fritz S, Eggen A, Bowman PJ, Coote D, Chamberlain AJ, Anderson C, VanTassell CP, Hulsegge I, Goddard ME, Guldbrandtsen B, Lund MS, Veerkamp RF, Boichard DA, Fries R, Hayes BJ. Whole-genome sequencing of 234 bulls facilitates mapping of monogenic and complex traits in cattle. Nat Genet 2014, advance online publication: doi:10.1038/ng.3034.
16. Xie Z, Ho WT, Exton JH. Association of the N- and C-terminal domains of phospholipase D: contribution of the conserved HKD motifs to the interaction and the requirement of the association for Ser/Thr phosphorylation of the enzyme. J Biol Chem 2000, 275:24962-24969. 10.1074/jbc.M909745199, 10825182.
17. Yoshikawa F, Banno Y, Otani Y, Yamaguchi Y, Nagakura-Takagi Y, Morita N, Sato Y, Saruta C, Nishibe H, Sadakata T, Shinoda Y, Hayashi K, Mishima Y, Baba H, Furuichi T. Phospholipase D family member 4, a transmembrane glycoprotein with no phospholipase D activity, expression in spleen and early postnatal microglia. PLoS One 2010, 5:e13932. 10.1371/journal.pone.0013932, 2978679, 21085684.
18. Trautwein G. Parakeratosis in black pied calves: 2: pathological findings. DTW Dtsch Tierarztl Wochenschr 1971, 78:265-270.
19. Maverakis E, Lynch PJ, Fazel N. Acrodermatitis enteropathica. Dermatol Online J 2007, 13:11.
20. O'Dell BL. Cysteine-rich intestinal protein (CRIP): a new intestinal zinc transport protein. Nutr Rev 1992, 50:232-233.
21. Cousins RJ. Gastrointestinal factors influencing zinc absorption and homeostasis. Int J Vitam Nutr Res 2010, 80:243-248. 10.1024/0300-9831/a000030, 3777256, 21462106.
22. Otani Y, Yamaguchi Y, Sato Y, Furuichi T, Ikenaka K, Kitani H, Baba H. PLD4 is involved in phagocytosis of microglia: expression and localization changes of PLD4 are correlated with activation state of microglia. PLoS One 2011, 6:e27544. 10.1371/journal.pone.0027544, 3216956, 22102906.
23. Terao C, Ohmura K, Kawaguchi Y, Nishimoto T, Kawasaki A, Takehara K, Furukawa H, Kochi Y, Ota Y, Ikari K, Sato S, Tohma S, Yamada R, Yamamoto K, Kubo M, Yamanaka H, Kuwana M, Tsuchiya N, Matsuda F, Mimori T. PLD4 as a novel susceptibility gene for systemic sclerosis in a Japanese population. Arthritis & Rheumatism 2013, 65:472-480. 10.1002/art.37777, 23124809.
24. Okada Y, Terao C, Ikari K, Kochi Y, Ohmura K, Suzuki A, Kawaguchi T, Stahl EA, Kurreeman FAS, Nishida N, Ohmiya H, Myouzen K, Takahashi M, Sawada T, Nishioka Y, Yukioka M, Matsubara T, Wakitani S, Teshima R, Tohma S, Takasugi K, Shimada K, Murasawa A, Honjo S, Matsuo K, Tanaka H, Tajima K, Suzuki T, Iwamoto T, Kawamura Y, et al. Meta-analysis identifies nine new loci associated with rheumatoid arthritis in the Japanese population. Nat Genet 2012, 44:511-516. 10.1038/ng.2231, 22446963.
25. Krieg T, Takehara K. Skin disease: a cardinal feature of systemic sclerosis. Rheumatology (Oxford) 2009, 3:iii14-18.
26. Picchianti Diamanti A, Germano V, Bizzi E, Laganà B, Migliore A. Interstitial lung disease in rheumatoid arthritis in the era of biologics. Pulm Med 2011, 2011:931342. 3250642, 22229089.
27. Bussone G, Mouthon L. Interstitial lung disease in systemic sclerosis. Autoimmun Rev 2011, 10:248-255. 10.1016/j.autrev.2010.09.012, 20863911.
28. Harris B, Ward-Bailey PF, Bergstrom DE, Bronson RT, Donahue LR. Thin hair with small size (thss) is a new recessive hair mutation on Chromosom 12 Bar Harbor, Maine: Mouse Mutant Resource Web Site, The Jackson Laboratory, (http://mousemutant.jax.org/). [September 17, 2012].
29. Arun SN, Xie D, Howard AC, Zhong Q, Zhong X, McNeil PL, Bollag WB. Cell wounding activates phospholipase D in primary mouse keratinocytes. J Lipid Res 2013, 54:581-591. 10.1194/jlr.M027060, 3617934, 23288946.
30. Grall A, Guaguère E, Planchais S, Grond S, Bourrat E, Hausser I, Hitte C, Le Gallo M, Derbois C, Kim G-J, Lagoutte L, Degorce-Rubiales F, Radner FPW, Thomas A, Küry S, Bensignor E, Fontaine J, Pin D, Zimmermann R, Zechner R, Lathrop M, Galibert F, André C, Fischer J. PNPLA1 mutations cause autosomal recessive congenital ichthyosis in golden retriever dogs and humans. Nat Genet 2012, 44:140-147. 10.1038/ng.1056, 22246504.
31. Frischmeyer PA, Dietz HC. Nonsense-mediated mRNA decay in health and disease. Hum Mol Genet 1999, 8:1893-1900. 10.1093/hmg/8.10.1893, 10469842.
32. Drögemüller C, Tetens J, Sigurdsson S, Gentile A, Testoni S, Lindblad-Toh K, Leeb T. Identification of the Bovine Arachnomelia Mutation by Massively Parallel Sequencing Implicates Sulfite Oxidase (SUOX) in bone development. PLoS Genet 2010, 6:e1001079. 10.1371/journal.pgen.1001079, 2928811, 20865119.
33. Gremme G, Brendel V, Sparks ME, Kurtz S. Engineering a software tool for gene structure prediction in higher organisms. Inform Software Tech 2005, 47:965-978.
34. Quackenbush J, Cho J, Lee D, Liang F, Holt I, Karamycheva S, Parvizi B, Pertea G, Sultana R, White J. The TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species. Nucl Acids Res 2001, 29:159-164. 10.1093/nar/29.1.159, 29813, 11125077.
35. Lewis SE, Searle SMJ, Harris N, Gibson M, Iyer V, Richter J, Wiel C, Bayraktaroglu L, Birney E, Crosby MA, Kaminker JS, Matthews BB, Prochnik SE, Smith CD, Tupy JL, Rubin GM, Misra S, Mungall CJ, Clamp ME. Apollo: a sequence annotation editor. Genome Biol 2002, 3:research0082. 1 - 0082.14, 151184, 12537571.
36. Ewing B, Green P. Base-calling of automated sequencer traces using phred: II: error probabilities. Genome Res 1998, 8:186-194.
37. Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using phred: I: accuracy assessment. Genome Res 1998, 8:175-185. 10.1101/gr.8.3.175, 9521921.
38. Nickerson DA, Tobe VO, Taylor SL. PolyPhred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing. Nucleic Acids Res 1997, 25:2745-2751. 10.1093/nar/25.14.2745, 146817, 9207020.
39. Gordon D, Abajian C, Green P. Consed: a graphical tool for sequence finishing. Genome Res 1998, 8:195-202. 10.1101/gr.8.3.195, 9521923.
40. Zimin AV, Delcher AL, Florea L, Kelley DR, Schatz MC, Puiu D, Hanrahan F, Pertea G, Van Tassell CP, Sonstegard TS, Marçais G, Roberts M, Subramanian P, Yorke JA, Salzberg SL. A whole-genome assembly of the domestic cow: bos taurus. Genome Biol 2009, 10:R42. 10.1186/gb-2009-10-4-r42, 2688933, 19393038.
41. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, Sham PC. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007, 81:559-575. 10.1086/519795, 1950838, 17701901.
42. Browning BL, Browning SR. A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am J Hum Genet 2009, 84:210-223. 10.1016/j.ajhg.2009.01.005, 2668004, 19200528.
43. Zhou X, Stephens M. Genome-wide efficient mixed-model analysis for association studies. Nat Genet 2012, 44:821-824. 10.1038/ng.2310, 3386377, 22706312.
44. VanRaden PM. Efficient methods to compute genomic predictions. J Dairy Sci 2008, 91:4414-4423. 10.3168/jds.2007-0980, 18946147.
45. Howie B, Fuchsberger C, Stephens M, Marchini J, Abecasis GR. Fast and accurate genotype imputation in genome-wide association studies through pre-phasing. Nat Genet 2012, 44:955-959. 10.1038/ng.2354, 3696580, 22820512.
46. Pausch H, Aigner B, Emmerling R, Edel C, Götz K-U, Fries R. Imputation of high-density genotypes in the Fleckvieh cattle population. Genet Sel Evol 2013, 45:3. 10.1186/1297-9686-45-3, 3598996, 23406470.
47. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760. 10.1093/bioinformatics/btp324, 2705234, 19451168.
48. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25:2078-2079. 10.1093/bioinformatics/btp352, 2723002, 19505943.
49. Li Y, Sidore C, Kang HM, Boehnke M, Abecasis GR. Low-coverage sequencing: implications for design of complex trait association studies. Genome Res 2011, 21:940-951. 10.1101/gr.117259.110, 3106327, 21460063.
50. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011, 43:491-498. 10.1038/ng.806, 3083463, 21478889.
51. Therneau TM, Grambsch PM. Modeling Survival Data: Extending the Cox Model 2000, New York: Springer.