Non-synonymous FGD3 Variant as Positional Candidate for Disproportional Tall Stature Accounting for a Carcass Weight QTL () and Skeletal Dysplasia in Japanese Black Cattle

English version České info

Livestock are typically subjected to intensive artificial selection for traits of economic value to producers. In spite of this strong selection, some major quantitative trait loci (QTLs) for an economically important trait never reach fixation in the population. Several studies have revealed that such QTLs are accompanied with an unfavorable effect on other traits of economic importance, including heritable disease phenotypes. The carcass weight QTL, named CW-3, was previously identified as one of three major QTL in Japanese Black cattle, and it was found to originate from a specific line that had been maintained in a regional subpopulation. Recent efforts to maintain genetic diversity of the Japanese Black breed have resulted in the widespread use of this line throughout Japan. Half-sib QTL analyses of the elite sires repeatedly detected the CW-3 QTL, while skeletal dysplasia has been found in the descendants. Genomic analyses revealed that skeletal dysplasia is inseparably linked with CW-3 and a functional variant of FGD3 was identified as a positional candidate QTN. Further studies such as creating a genetically modified mouse model will be useful to understand a molecular mechanism of FGD3 to modulate bone development.

Vyšlo v časopise: Non-synonymous FGD3 Variant as Positional Candidate for Disproportional Tall Stature Accounting for a Carcass Weight QTL () and Skeletal Dysplasia in Japanese Black Cattle. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005433
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005433

Souhrn

Zdroje

1. Mikawa S, Morozumi T, Shimanuki S, Hayashi T, Uenishi H, Domukai M. et al. Fine mapping of a swine quantitative trait locus for number of vertebrae and analysis of an orphan nuclear receptor, germ cell nuclear factor (NR6A1). Genome Res. 2007; 17: 586–593. 17416745

2. Setoguchi K, Furuta M, Hirano T, Nagao T, Watanabe T, Sugimoto Y. et al. Cross-breed comparisons identified a critical 591 kb region for bovine carcass weight QTL (CW-2) on chromosome 6 and the Ile-442-Met substitution in NCAPG as a positional candidate. BMC Genetics. 2009; 10: 43. doi: 10.1186/1471-2156-10-43 19653884

3. Karim L, Takeda H, Lin L, Druet T, Arias JA, Baurain D. et al. Variants modulating the expression of a chromosome domain encompassing PLAG1 influence bovine stature. Nat Genet. 2011; 43: 405–413. doi: 10.1038/ng.814 21516082

4. Wood AR, Esko T, Yang J, Vedantam S, Pers TH, Gustafsson S. et al. Defining the role of common variation in the genomic and biological architecture of adult human height. Nat Genet. 2014; 46: 1173–1186. doi: 10.1038/ng.3097 25282103

5. Rubin CJ, Megens HJ, Martinez Barrio A, Maqbool K, Sayyab S, Schwochow D. et al. Strong signatures of selection in the domestic pig genome. Proc Natl Acad Sci U S A. 2012; 109: 19529–19536. doi: 10.1073/pnas.1217149109 23151514

6. Saatchi M, Schnabel RD, Taylor JF, Garrick DJ. Large-effect pleiotropic or closely linked QTL segregate within and across ten US cattle breeds. BMC Genomics. 2014; 15: 442. doi: 10.1186/1471-2164-15-442 24906442

7. Nishimura S, Watanabe T, Mizoshita K, Tatsuda K, Fujita T, Watanabe N. et al. Genome-wide association study identified three major QTL for carcass weight including the PLAG1-CHCHD7 QTN for stature in Japanese Black cattle. BMC Genet. 2012; 13: 40. doi: 10.1186/1471-2156-13-40 22607022

8. Gudbjartsson DF, Walters GB, Thorleifsson G, Stefansson H, Halldorsson BV, Zusmanovich P. et al. Many sequence variants affecting diversity of adult human height. Nat Genet. 2008; 40: 609–615. doi: 10.1038/ng.122 18391951

9. Lettre G, Jackson AU, Gieger C, Schumacher FR, Berndt SI, Sanna S et al. Identification of ten loci associated with height highlights new biological pathways in human growth. Nat Genet. 2008; 40: 584–591. doi: 10.1038/ng.125 18391950

10. Weedon MN, Lango H, Lindgren CM, Wallace C, Evans DM, Mangino M. et al. Genome-wide association analysis identifies 20 loci that influence adult height. Nat Genet. 2008; 40: 575–583. doi: 10.1038/ng.121 18391952

11. Takasuga A. Stature QTLs in livestock animals. Anim. Sci. J. 2015.

12. Grisart B, Coppieters W, Farnir F, Karim L, Ford C, Berzi P. et al. Positional candidate cloning of a QTL in dairy cattle: identification of a missense mutation in the bovine DGAT1 gene with major effect on milk yield and composition. Genome Res. 2001; 12: 222–231.

13. Fasquelle C, Sartelet A, Li W, Dive M, Tamma N, Michaux C. et al. Balancing selection of a frame-shift mutation in the MRC2 gene accounts for the outbreak of the Crooked Tail Syndrome in Belgian Blue Cattle. PLoS Genet. 2009; 5: e1000666. doi: 10.1371/journal.pgen.1000666 19779552

14. Charlier C, Coppieters W, Rollin F, Desmecht D, Agerholm JS, Cambisano N, et al. Highly effective SNP-based association mapping and management of recessive defects in livestock. Nat Genet. 2008; 40: 449–454. doi: 10.1038/ng.96 18344998

15. Hirano T, Kobayashi N, Matsuhashi T, Watanabe D, Watanabe T, Takasuga A, et al. Mapping and exome sequencing identifies a mutation in the IARS gene as the cause of hereditary perinatal weak calf syndrome. PLoS One. 2013; 8: e64036. doi: 10.1371/journal.pone.0064036 23700453

16. Hoshiba H, Setoguchi K, Watanabe T, Kinoshita A, Mizoshita K, Sugimoto Y. et al. Comparison of the effects explained by variations in the bovine PLAG1 and NCAPG genes on daily body weight gain, linear skeletal measurements and carcass traits in Japanese Black steers from a progeny testing program. Anim Sci Journal. 2013; 84: 529–534.

17. Setoguchi K, Watanabe T, Weikard R, Albrecht E, Kühn C, Kinoshita A. et al. The SNP c.1326T>G in the non-SMC condensin I complex, subunit G (NCAPG) gene encoding a p.Ile442Met variant is associated with an increase in body frame size at puberty in cattle. Anim Genet. 2011; 42: 650–655. doi: 10.1111/j.1365-2052.2011.02196.x 22035007

18. Neveling K, Martinez-Carrera LA, Hölker I, Heister A, Verrips A, Hosseini-Barkooie SM, et al. Mutations in BICD2, which encodes a golgin and important motor adaptor, cause congenital autosomal-dominant spinal muscular atrophy. Am J Hum Genet. 2013; 92: 946–954. doi: 10.1016/j.ajhg.2013.04.011 23664116

19. Peeters K, Litvinenko I, Asselbergh B, Almeida-Souza L, Chamova T, Geuens T, et al. Molecular defects in the motor adaptor BICD2 cause proximal spinal muscular atrophy with autosomal-dominant inheritance. Am J Hum Genet. 2013; 92: 955–964. doi: 10.1016/j.ajhg.2013.04.013 23664119

20. Oates EC, Rossor AM, Hafezparast M, Gonzalez M, Speziani F, MacArthur DG, et al. Mutations in BICD2 cause dominant congenital spinal muscular atrophy and hereditary spastic paraplegia. Am J Hum Genet. 2013; 92: 965–973. doi: 10.1016/j.ajhg.2013.04.018 23664120

21. Lango Allen H, Estrada K, Lettre G, Berndt SI, Weedon MN, Rivadeneira F. et al. Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature. 2010; 467: 832–838. doi: 10.1038/nature09410 20881960

22. Goodrich LV, Milenković L, Higgins KM, Scott MP. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science. 1997; 277: 1109–1113. 9262482

23. Takasuga A, Watanabe T, Mizoguchi Y, Hirano T, Ihara N, Takano A, et al. Identification of bovine QTL for growth and carcass traits in Japanese Black cattle by replication and identical-by-descent mapping. Mamm Genome. 2007; 18: 125–136. 17347893

24. Hayakawa M, Matsushima M, Hagiwara H, Oshima T, Fujino T, Ando K, et al. Novel insights into FGD3, a putative GEF for Cdc42, that undergoes SCF(FWD1/beta-TrCP)-mediated proteasomal degradation analogous to that of its homologue FGD1 but regulates cell morphology and motility differently from FGD1. Genes Cells. 2008; 13: 329–342. doi: 10.1111/j.1365-2443.2008.01168.x 18363964

25. Pasteris NG, Cadle A, Logie LJ, Porteous MEM, Schwartz CE, Stevenson RE, et al. Isolation and analysis of the faciogenital dysplasia (Aarskog-Scott syndrome) gene: a putative, rho/rac guanine nucleotide exchange factor. Cell. 1994; 79: 669–678. 7954831

26. Gorski JL, Estrada L, Hu C, Liu Z. Skeletal-specific expression of Fgd1 during bone formation and skeletal defects in faciogenital dysplasia (FGDY; Aarskog syndrome). Dev Dyn. 2000; 218: 573–586. 10906777

27. Steenblock C, Heckel T, Czupalla C, Espírito Santo AI, Niehage C, Sztacho M, et al. The Cdc42 guanine nucleotide exchange factor FGD6 coordinates cell polarity and endosomal membrane recycling in osteoclasts. J Biol Chem. 2014; 289: 18347–18359. doi: 10.1074/jbc.M113.504894 24821726

28. Lacroix L, Lazar V, Michiels S, Ripoche H, Dessen P, Talbot M, et al. Follicular thyroid tumors with the PAX8-PPARgamma1 rearrangement display characteristic genetic alterations. Am J Pathol. 2005; 167: 223–231. 15972966

29. Aizawa R, Yamada A, Suzuki D, Iimura T, Kassai H, Harada T, et al. Cdc42 is required for chondrogenesis and interdigital programmed cell death during limb development. Mech Dev. 2012; 129: 38–50. doi: 10.1016/j.mod.2012.02.002 22387309

30. Suzuki W, Yamada A, Aizawa R, Suzuki D, Kassai H, Harada T, et al. Cdc42 is critical for cartilage development during endochondral ossification. Endocrinology. 2015; 156: 314–22. doi: 10.1210/en.2014-1032 25343271

31. Yasoda A, Ogawa Y, Suda M, Tamura N, Mori K, Sakuma Y, et al. Natriuretic peptide regulation of endochondral ossification. Evidence for possible roles of the C-type natriuretic peptide/guanylyl cyclase-B pathway. J Biol Chem. 1998; 273: 11695–11700. 9565590

32. Chikuda H, Kugimiya F, Hoshi K, Ikeda T, Ogasawara T, Shimoaka T, et al. Cyclic GMP-dependent protein kinase II is a molecular switch from proliferation to hypertrophic differentiation of chondrocytes. Genes Dev. 2004; 18: 2418–2429. 15466490

33. Tsuji T, Kunieda T. A loss-of-function mutation in natriuretic peptide receptor 2 (Npr2) gene is responsible for disproportionate dwarfism in cn/cn mouse. J Biol Chem. 2005; 280:14288–14292. 15722353

34. Miura K, Namba N, Fujiwara M, Ohata Y, Ishida H, Kitaoka T, et al. An overgrowth disorder associated with excessive production of cGMP due to a gain-of-function mutation of the natriuretic peptide receptor 2 gene. PLoS One. 2012; 7: e42180. doi: 10.1371/journal.pone.0042180 22870295

35. Matsukawa N, Grzesik WJ, Takahashi N, Pandey KN, Pang S, Yamauchi M, et al. The natriuretic peptide clearance receptor locally modulates the physiological effects of the natriuretic peptide system. Proc Natl Acad Sci U S A. 1999; 96: 7403–7408. 10377427

36. Ihara N, Takasuga A, Mizoshita K, Takeda H, Sugimoto M, Mizoguchi Y, et al. A comprehensive genetic map of the cattle genome based on 3802 microsatellites. Genome Res. 2004; 14: 1987–1998. 15466297

37. Untergrasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3—new capabilities and interfaces. Nucleic Acids Res. 2012; 40: e115. 22730293

38. Browning SR, Browning BL. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet. 2007; 81: 1084–1097. 17924348

39. Kang HM, Sul JH, Service SK, Zaitlen NA, Kong SY, Freimer NB, et al. Variance component model to account for sample structure in genome-wide association studies. Nat Genet. 2010; 42: 348–354. doi: 10.1038/ng.548 20208533

40. Hirano T, Kobayashi N, Itoh T, Takasuga A, Nakamaru T, Hirotsune S, et al. Null mutation of PCLN-1/Claudin-16 results in bovine chronic interstitial nephritis. Genome Res. 2000; 10: 659–663. 10810088

41. Niwa H, Yamamura K, Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene. 1991; 108: 193–200. 1660837

42. Japan Wagyu Register Association: Kurogewashu seijyo hatsuiku kyokusen. Japan Wagyu Register Association; 2004.