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Akirin proteins in development and disease: critical roles and mechanisms of action

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Abstract

The Akirin genes, which encode small, nuclear proteins, were first characterized in 2008 in Drosophila and rodents. Early studies demonstrated important roles in immune responses and tumorigenesis, which subsequent work found to be highly conserved. More recently, a multiplicity of Akirin functions, and the associated molecular mechanisms involved, have been uncovered. Here, we comprehensively review what is known about invertebrate Akirin and its two vertebrate homologues Akirin1 and Akirin2, highlighting their role in regulating gene expression changes across a number of biological systems. We detail essential roles for Akirin family proteins in the development of the brain, limb, and muscle, in meiosis, and in tumorigenesis, emphasizing associated signaling pathways. We describe data supporting the hypothesis that Akirins act as a “bridge” between a variety of transcription factors and major chromatin remodeling complexes, and discuss several important questions remaining to be addressed. In little more than a decade, Akirin proteins have gone from being completely unknown to being increasingly recognized as evolutionarily conserved mediators of gene expression programs essential for the formation and function of animals.

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References

  1. Tartey S, Takeuchi O (2015) Chromatin remodeling and transcriptional control in innate immunity: emergence of Akirin2 as a novel player. Biomolecules 5(3):1618–1633. https://doi.org/10.3390/biom5031618

    Article  CAS  Google Scholar 

  2. Tartey S, Takeuchi O (2016) Akirin2-mediated transcriptional control by recruiting SWI/SNF complex in B Cells. Crit Rev Immunol 36(5):395–406. https://doi.org/10.1615/CritRevImmunol.2017019629

    Article  Google Scholar 

  3. Artigas-Jeronimo S, Villar M, Cabezas-Cruz A, Valdes JJ, Estrada-Pena A, Alberdi P, de la Fuente J (2018) Functional evolution of subolesin/akirin. Front Physiol 9:1612. https://doi.org/10.3389/fphys.2018.01612

    Article  Google Scholar 

  4. Macqueen DJ, Johnston IA (2009) Evolution of the multifaceted eukaryotic akirin gene family. BMC Evol Biol 9:34. https://doi.org/10.1186/1471-2148-9-34

    Article  CAS  Google Scholar 

  5. Macqueen DJ, Kristjansson BK, Johnston IA (2010) Salmonid genomes have a remarkably expanded akirin family, coexpressed with genes from conserved pathways governing skeletal muscle growth and catabolism. Physiol Genom 42(1):134–148. https://doi.org/10.1152/physiolgenomics.00045.2010

    Article  CAS  Google Scholar 

  6. Goto A, Matsushita K, Gesellchen V, El Chamy L, Kuttenkeuler D, Takeuchi O, Hoffmann JA, Akira S, Boutros M, Reichhart JM (2008) Akirins are highly conserved nuclear proteins required for NF-kappaB-dependent gene expression in drosophila and mice. Nat Immunol 9(1):97–104. https://doi.org/10.1038/ni1543

    Article  CAS  Google Scholar 

  7. Almazan C, Kocan KM, Bergman DK, Garcia-Garcia JC, Blouin EF, de la Fuente J (2003) Identification of protective antigens for the control of Ixodes scapularis infestations using cDNA expression library immunization. Vaccine 21(13–14):1492–1501. https://doi.org/10.1016/s0264-410x(02)00683-7

    Article  CAS  Google Scholar 

  8. de la Fuente J, Almazan C, Blas-Machado U, Naranjo V, Mangold AJ, Blouin EF, Gortazar C, Kocan KM (2006) The tick protective antigen, 4D8, is a conserved protein involved in modulation of tick blood ingestion and reproduction. Vaccine 24(19):4082–4095. https://doi.org/10.1016/j.vaccine.2006.02.046

    Article  CAS  Google Scholar 

  9. Nowak SJ, Aihara H, Gonzalez K, Nibu Y, Baylies MK (2012) Akirin links twist-regulated transcription with the Brahma chromatin remodeling complex during embryogenesis. PLoS Genet 8(3):e1002547. https://doi.org/10.1371/journal.pgen.1002547

    Article  CAS  Google Scholar 

  10. Marshall A, Salerno MS, Thomas M, Davies T, Berry C, Dyer K, Bracegirdle J, Watson T, Dziadek M, Kambadur R et al (2008) Mighty is a novel promyogenic factor in skeletal myogenesis. Exp Cell Res 314(5):1013–1029. https://doi.org/10.1016/j.yexcr.2008.01.004

    Article  CAS  Google Scholar 

  11. Komiya Y, Kurabe N, Katagiri K, Ogawa M, Sugiyama A, Kawasaki Y, Tashiro F (2008) A novel binding factor of 14-3-3beta functions as a transcriptional repressor and promotes anchorage-independent growth, tumorigenicity, and metastasis. J Biol Chem 283(27):18753–18764. https://doi.org/10.1074/jbc.M802530200

    Article  CAS  Google Scholar 

  12. Clemons AM, Brockway HM, Yin Y, Kasinathan B, Butterfield YS, Jones SJ, Colaiacovo MP, Smolikove S (2013) Akirin is required for diakinesis bivalent structure and synaptonemal complex disassembly at meiotic prophase I. Mol Biol Cell 24(7):1053–1067. https://doi.org/10.1091/mbc.E12-11-0841

    Article  CAS  Google Scholar 

  13. Bowman R, Balukoff N, Clemons A, Koury E, Ford T, Baxi K, de Carvalho CE, Smolikove S (2019) Akirin is required for muscle function and acts through the TGF-beta Sma/Mab signaling pathway in Caenorhabditis elegans development. G3 (Bethesda) 1:1. https://doi.org/10.1534/g3.119.400377

    Article  CAS  Google Scholar 

  14. Tartey S, Matsushita K, Vandenbon A, Ori D, Imamura T, Mino T, Standley DM, Hoffmann JA, Reichhart JM, Akira S et al (2014) Akirin2 is critical for inducing inflammatory genes by bridging IkappaB-zeta and the SWI/SNF complex. EMBO J 33(20):2332–2348. https://doi.org/10.15252/embj.201488447

    Article  CAS  Google Scholar 

  15. Crosby MA, Goodman JL, Strelets VB, Zhang P, Gelbart WM (2007) FlyBase: genomes by the dozen. Nucleic Acids Res 35:D486–491. https://doi.org/10.1093/nar/gkl827

    Article  CAS  Google Scholar 

  16. Chintapalli VR, Wang J, Dow JA (2007) Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 39(6):715–720. https://doi.org/10.1038/ng2049

    Article  CAS  Google Scholar 

  17. Bonnay F, Nguyen XH, Cohen-Berros E, Troxler L, Batsche E, Camonis J, Takeuchi O, Reichhart JM, Matt N (2014) Akirin specifies NF-kappaB selectivity of Drosophila innate immune response via chromatin remodeling. EMBO J 33(20):2349–2362. https://doi.org/10.15252/embj.201488456

    Article  CAS  Google Scholar 

  18. Polanowska J, Chen JX, Soule J, Omi S, Belougne J, Taffoni C, Pujol N, Selbach M, Zugasti O, Ewbank JJ (2018) Evolutionary plasticity in the innate immune function of Akirin. PLoS Genet 14(7):e1007494. https://doi.org/10.1371/journal.pgen.1007494

    Article  CAS  Google Scholar 

  19. Hunt-Newbury R, Viveiros R, Johnsen R, Mah A, Anastas D, Fang L, Halfnight E, Lee D, Lin J, Lorch A et al (2007) High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol 5(9):e237. https://doi.org/10.1371/journal.pbio.0050237

    Article  CAS  Google Scholar 

  20. Hefel A, Smolikove S (2019) Tissue-specific split sfGFP system for streamlined expression of GFP tagged proteins in the Caenorhabditis elegans germline. G3 (Bethesda) 9(6):1933–1943. https://doi.org/10.1534/g3.119.400162

    Article  CAS  Google Scholar 

  21. Bowman R, Balukof N, Ford T, Smolikove S (2019) A novel role for alpha-importins and akirin in establishment of meiotic sister chromatid cohesion in Caenorhabditis elegans. Genetics 211(2):617–635. https://doi.org/10.1534/genetics.118.301458

    Article  CAS  Google Scholar 

  22. Liu X, Xia Y, Tang J, Ma L, Li C, Ma P, Mao B (2017) Dual roles of Akirin2 protein during Xenopus neural development. J Biol Chem 292(14):5676–5684. https://doi.org/10.1074/jbc.M117.777110

    Article  CAS  Google Scholar 

  23. Yue F, Cheng Y, Breschi A, Vierstra J, Wu W, Ryba T, Sandstrom R, Ma Z, Davis C, Pope BD et al (2014) A comparative encyclopedia of DNA elements in the mouse genome. Nature 515(7527):355–364. https://doi.org/10.1038/nature13992

    Article  CAS  Google Scholar 

  24. Tartey S, Matsushita K, Imamura T, Wakabayashi A, Ori D, Mino T, Takeuchi O (2015) Essential function for the nuclear protein Akirin2 in B cell activa. J Immunol (Baltimore, Md : 1950) 195(2):519–527. https://doi.org/10.4049/jimmunol.1500373

    Article  CAS  Google Scholar 

  25. Bosch PJ, Fuller LC, Sleeth CM, Weiner JA (2016) Akirin2 is essential for the formation of the cerebral cortex. Neural Dev 11(1):21. https://doi.org/10.1186/s13064-016-0076-8

    Article  CAS  Google Scholar 

  26. Bosch PJ, Fuller LC, Weiner JA (2019) A critical role for the nuclear protein Akirin2 in the formation of mammalian muscle in vivo. Genesis (New York, NY : 2000) 57(5):e23286. https://doi.org/10.1002/dvg.23286

    Article  CAS  Google Scholar 

  27. Bosch PJ, Fuller LC, Weiner JA (2018) An essential role for the nuclear protein Akirin2 in mouse limb interdigital tissue regression. Sci Rep 8(1):12240. https://doi.org/10.1038/s41598-018-30801-2

    Article  CAS  Google Scholar 

  28. Fagerberg L, Hallstrom BM, Oksvold P, Kampf C, Djureinovic D, Odeberg J, Habuka M, Tahmasebpoor S, Danielsson A, Edlund K et al (2014) Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol Cell Proteomics 13(2):397–406. https://doi.org/10.1074/mcp.M113.035600

    Article  CAS  Google Scholar 

  29. Coulibaly A, Velasquez SY, Sticht C, Figueiredo AS, Himmelhan BS, Schulte J, Sturm T, Centner FS, Schottler JJ, Thiel M et al (2019) AKIRIN1: a potential new reference gene in human natural killer cells and granulocytes in sepsis. Int J Mol Sci. https://doi.org/10.3390/ijms20092290

    Article  Google Scholar 

  30. Leng K, Xu Y, Kang P, Qin W, Cai H, Wang H, Ji D, Jiang X, Li J, Li Z et al (2019) Akirin2 is modulated by miR-490-3p and facilitates angiogenesis in cholangiocarcinoma through the IL-6/STAT3/VEGFA signaling pathway. Cell Death Dis 10(4):262. https://doi.org/10.1038/s41419-019-1506-4

    Article  CAS  Google Scholar 

  31. Krossa S, Schmitt AD, Hattermann K, Fritsch J, Scheidig AJ, Mehdorn HM, Held-Feindt J (2015) Down regulation of Akirin-2 increases chemosensitivity in human glioblastomas more efficiently than Twist-1. Oncotarget 6(25):21029–21045

    Article  Google Scholar 

  32. Akiyama H, Iwahana Y, Suda M, Yoshimura A, Kogai H, Nagashima A, Ohtsuka H, Komiya Y, Tashiro F (2013) The FBI1/Akirin2 target gene, BCAM, acts as a suppressive oncogene. PLoS ONE 8(11):e78716. https://doi.org/10.1371/journal.pone.0078716

    Article  CAS  Google Scholar 

  33. Pulice JL, Kadoch C (2016) Composition and function of mammalian SWI/SNF chromatin remodeling complexes in human disease. Cold Spring Harb Symp Quant Biol 81:53–60. https://doi.org/10.1101/sqb.2016.81.031021

    Article  Google Scholar 

  34. Tang L, Nogales E, Ciferri C (2010) Structure and function of SWI/SNF chromatin remodeling complexes and mechanistic implications for transcription. Prog Biophys Mol Biol 102(2–3):122–128. https://doi.org/10.1016/j.pbiomolbio.2010.05.001

    Article  CAS  Google Scholar 

  35. Cairns BR (2007) Chromatin remodeling: insights and intrigue from single-molecule studies. Nat Struct Mol Biol 14(11):989–996. https://doi.org/10.1038/nsmb1333

    Article  CAS  Google Scholar 

  36. Gao X, Tate P, Hu P, Tjian R, Skarnes WC, Wang Z (2008) ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. Proc Natl Acad Sci USA 105(18):6656–6661. https://doi.org/10.1073/pnas.0801802105

    Article  Google Scholar 

  37. Vazquez M, Moore L, Kennison JA (1999) The trithorax group gene osa encodes an ARID-domain protein that genetically interacts with the brahma chromatin-remodeling factor to regulate transcription. Development (Cambridge, England) 126(4):733–742

    CAS  Google Scholar 

  38. Giot L, Bader JS, Brouwer C, Chaudhuri A, Kuang B, Li Y, Hao YL, Ooi CE, Godwin B, Vitols E et al (2003) A protein interaction map of Drosophila melanogaster. Science (New York, NY) 302(5651):1727–1736. https://doi.org/10.1126/science.1090289

    Article  CAS  Google Scholar 

  39. Wright PE, Dyson HJ (2015) Intrinsically disordered proteins in cellular signalling and regulation. Nat Rev Mol Cell Biol 16(1):18–29. https://doi.org/10.1038/nrm3920

    Article  CAS  Google Scholar 

  40. Nowak SJ, Baylies MK (2012) Akirin: a context-dependent link between transcription and chromatin remodeling. Bioarchitecture 2(6):209–213. https://doi.org/10.4161/bioa.22907

    Article  Google Scholar 

  41. Gilmore TD (2006) Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 25(51):6680–6684. https://doi.org/10.1038/sj.onc.1209954

    Article  CAS  Google Scholar 

  42. Trinh DV, Zhu N, Farhang G, Kim BJ, Huxford T (2008) The nuclear I kappaB protein I kappaB zeta specifically binds NF-kappaB p50 homodimers and forms a ternary complex on kappaB DNA. J Mol Biol 379(1):122–135. https://doi.org/10.1016/j.jmb.2008.03.060

    Article  CAS  Google Scholar 

  43. Carmona-Mora P, Widagdo J, Tomasetig F, Canales CP, Cha Y, Lee W, Alshawaf A, Dottori M, Whan RM, Hardeman EC et al (2015) The nuclear localization pattern and interaction partners of GTF2IRD1 demonstrate a role in chromatin regulation. Hum Genet 134(10):1099–1115. https://doi.org/10.1007/s00439-015-1591-0

    Article  CAS  Google Scholar 

  44. Yan J, Dong X, Kong Y, Zhang Y, Jing R, Feng L (2013) Identification and primary immune characteristics of an amphioxus akirin homolog. Fish Shellfish Immunol 35(2):564–571. https://doi.org/10.1016/j.fsi.2013.05.020

    Article  CAS  Google Scholar 

  45. Liu N, Wang XW, Sun JJ, Wang L, Zhang HW, Zhao XF, Wang JX (2016) Akirin interacts with Bap60 and 14-3-3 proteins to regulate the expression of antimicrobial peptides in the kuruma shrimp (Marsupenaeus japonicus). Dev Comp Immunol 55:80–89. https://doi.org/10.1016/j.dci.2015.10.015

    Article  CAS  Google Scholar 

  46. Freeman AK, Morrison DK (2011) 14-3-3 Proteins: diverse functions in cell proliferation and cancer progression. Semin Cell Dev Biol 22(7):681–687. https://doi.org/10.1016/j.semcdb.2011.08.009

    Article  CAS  Google Scholar 

  47. Deaton AM, Bird A (2011) CpG islands and the regulation of transcription. Genes Dev 25(10):1010–1022. https://doi.org/10.1101/gad.2037511

    Article  CAS  Google Scholar 

  48. Goto A, Fukuyama H, Imler JL, Hoffmann JA (2014) The chromatin regulator DMAP1 modulates activity of the nuclear factor B (NF-B) transcription factor Relish in the Drosophila innate immune response. J Biol Chem 289(30):20470–20476. https://doi.org/10.1074/jbc.C114.553719

    Article  CAS  Google Scholar 

  49. Penicud K, Behrens A (2014) DMAP1 is an essential regulator of ATM activity and function. Oncogene 33(4):525–531. https://doi.org/10.1038/onc.2012.597

    Article  CAS  Google Scholar 

  50. Murphy LO, Blenis J (2006) MAPK signal specificity: the right place at the right time. Trends Biochem Sci 31(5):268–275. https://doi.org/10.1016/j.tibs.2006.03.009

    Article  CAS  Google Scholar 

  51. Komiya Y, Akiyama H, Sakumoto R, Tashiro F (2014) FBI1/Akirin2 promotes tumorigenicity and metastasis of Lewis lung carcinoma cells. Biochem Biophys Res Commun 444(3):382–386. https://doi.org/10.1016/j.bbrc.2014.01.064

    Article  CAS  Google Scholar 

  52. Chen X, Luo Y, Huang Z, Jia G, Liu G, Zhao H (2017) Akirin2 regulates proliferation and differentiation of porcine skeletal muscle satellite cells via ERK1/2 and NFATc1 signaling pathways. Sci Rep 7:45156. https://doi.org/10.1038/srep45156

    Article  CAS  Google Scholar 

  53. Chen X, Guo Y, Jia G, Zhao H, Liu G, Huang Z (2018) Arginine promotes slow myosin heavy chain expression via Akirin2 and the AMP-activated protein kinase signaling pathway in porcine skeletal muscle satellite cells. J Agric Food Chem 66(18):4734–4740. https://doi.org/10.1021/acs.jafc.8b00775

    Article  CAS  Google Scholar 

  54. Rao VV, Sangiah U, Mary KA, Akira S, Mohanty A (2019) Role of Akirin1 in the regulation of skeletal muscle fiber-type switch. J Cell Biochem. https://doi.org/10.1002/jcb.28406

    Article  Google Scholar 

  55. Salerno MS, Dyer K, Bracegirdle J, Platt L, Thomas M, Siriett V, Kambadur R, Sharma M (2009) Akirin1 (Mighty), a novel promyogenic factor regulates muscle regeneration and cell chemotaxis. Exp Cell Res 315(12):2012–2021. https://doi.org/10.1016/j.yexcr.2009.04.014

    Article  CAS  Google Scholar 

  56. Gumienny TL, Savage-Dunn C (2013) TGF-beta signaling in C. elegans. WormBook. https://doi.org/10.1895/wormbook.1.22.2

    Article  Google Scholar 

  57. Guo B, Huang X, Zhang P, Qi L, Liang Q, Zhang X, Huang J, Fang B, Hou W, Han J et al (2014) Genome-wide screen identifies signaling pathways that regulate autophagy during Caenorhabditis elegans development. EMBO Rep 15(6):705–713. https://doi.org/10.1002/embr.201338310

    Article  CAS  Google Scholar 

  58. Clark JF, Meade M, Ranepura G, Hall DH, Savage-Dunn C (2018) Caenorhabditis elegans DBL-1/BMP regulates lipid accumulation via interaction with insulin signaling. G3 (Bethesda) 8(1):343–351. https://doi.org/10.1534/g3.117.300416

    Article  CAS  Google Scholar 

  59. Morita K, Chow KL, Ueno N (1999) Regulation of body length and male tail ray pattern formation of Caenorhabditis elegans by a member of TGF-beta family. Development (Cambridge, England) 126(6):1337–1347

    CAS  Google Scholar 

  60. Baldin V, Lukas J, Marcote MJ, Pagano M, Draetta G (1993) Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev 7(5):812–821

    Article  CAS  Google Scholar 

  61. Seo S, Herr A, Lim JW, Richardson GA, Richardson H, Kroll KL (2005) Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev 19(14):1723–1734. https://doi.org/10.1101/gad.1319105

    Article  CAS  Google Scholar 

  62. Lessard J, Wu JI, Ranish JA, Wan M, Winslow MM, Staahl BT, Wu H, Aebersold R, Graef IA, Crabtree GR (2007) An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55(2):201–215. https://doi.org/10.1016/j.neuron.2007.06.019

    Article  CAS  Google Scholar 

  63. Ronan JL, Wu W, Crabtree GR (2013) From neural development to cognition: unexpected roles for chromatin. Nat Rev Genet 14(5):347–359. https://doi.org/10.1038/nrg3413

    Article  CAS  Google Scholar 

  64. Conaco C, Otto S, Han JJ, Mandel G (2006) Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci USA 103(7):2422–2427. https://doi.org/10.1073/pnas.0511041103

    Article  CAS  Google Scholar 

  65. Yoo AS, Staahl BT, Chen L, Crabtree GR (2009) MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460(7255):642–646. https://doi.org/10.1038/nature08139

    Article  CAS  Google Scholar 

  66. Ooi L, Belyaev ND, Miyake K, Wood IC, Buckley NJ (2006) BRG1 chromatin remodeling activity is required for efficient chromatin binding by repressor element 1-silencing transcription factor (REST) and facilitates REST-mediated repression. J Biol Chem 281(51):38974–38980. https://doi.org/10.1074/jbc.M605370200

    Article  CAS  Google Scholar 

  67. Staahl BT, Crabtree GR (2013) Creating a neural specific chromatin landscape by npBAF and nBAF complexes. Curr Opin Neurobiol 23(6):903–913. https://doi.org/10.1016/j.conb.2013.09.003

    Article  CAS  Google Scholar 

  68. Matsumoto S, Banine F, Struve J, Xing R, Adams C, Liu Y, Metzger D, Chambon P, Rao MS, Sherman LS (2006) Brg1 is required for murine neural stem cell maintenance and gliogenesis. Dev Biol 289(2):372–383. https://doi.org/10.1016/j.ydbio.2005.10.044

    Article  CAS  Google Scholar 

  69. Santen GW, Aten E, Sun Y, Almomani R, Gilissen C, Nielsen M, Kant SG, Snoeck IN, Peeters EA, Hilhorst-Hofstee Y et al (2012) Mutations in SWI/SNF chromatin remodeling complex gene ARID1B cause Coffin-Siris syndrome. Nat Genet 44(4):379–380. https://doi.org/10.1038/ng.2217

    Article  CAS  Google Scholar 

  70. Tsurusaki Y, Okamoto N, Ohashi H, Kosho T, Imai Y, Hibi-Ko Y, Kaname T, Naritomi K, Kawame H, Wakui K et al (2012) Mutations affecting components of the SWI/SNF complex cause Coffin–Siris syndrome. Nat Genet 44(4):376–378. https://doi.org/10.1038/ng.2219

    Article  CAS  Google Scholar 

  71. Florio M, Huttner WB (2014) Neural progenitors, neurogenesis and the evolution of the neocortex. Development (Cambridge, England) 141(11):2182–2194. https://doi.org/10.1242/dev.090571

    Article  CAS  Google Scholar 

  72. Engwerda A, Frentz B, den Ouden AL, Flapper BCT, Swertz MA, Gerkes EH, Plantinga M, Dijkhuizen T, van Ravenswaaij-Arts CMA (2018) The phenotypic spectrum of proximal 6q deletions based on a large cohort derived from social media and literature reports. Eur J Hum Genet EJHG 26(10):1478–1489. https://doi.org/10.1038/s41431-018-0172-9

    Article  CAS  Google Scholar 

  73. Philogene MC, Small SG, Wang P, Corsi AK (2012) Distinct Caenorhabditis elegans HLH-8/twist-containing dimers function in the mesoderm. Dev Dyn 241(3):481–492. https://doi.org/10.1002/dvdy.23734

    Article  CAS  Google Scholar 

  74. Forcales SV, Albini S, Giordani L, Malecova B, Cignolo L, Chernov A, Coutinho P, Saccone V, Consalvi S, Williams R et al (2012) Signal-dependent incorporation of MyoD-BAF60c into Brg1-based SWI/SNF chromatin-remodelling complex. EMBO J 31(2):301–316. https://doi.org/10.1038/emboj.2011.391

    Article  CAS  Google Scholar 

  75. Chen X, Luo Y, Zhou B, Huang Z, Jia G, Liu G, Zhao H, Yang Z, Zhang R (2015) Effect of porcine Akirin2 on skeletal myosin heavy chain isoform expression. Int J Mol Sci 16(2):3996–4006. https://doi.org/10.3390/ijms16023996

    Article  CAS  Google Scholar 

  76. Chen X, Luo Y, Huang Z, Liu G, Zhao H (2017) Akirin2 promotes slow myosin heavy chain expression by CaN/NFATc1 signaling in porcine skeletal muscle satellite cells. Oncotarget 8(15):25158–25166. https://doi.org/10.18632/oncotarget.15374

    Article  Google Scholar 

  77. Sasaki S, Yamada T, Sukegawa S, Miyake T, Fujita T, Morita M, Ohta T, Takahagi Y, Murakami H, Morimatsu F et al (2009) Association of a single nucleotide polymorphism in akirin 2 gene with marbling in Japanese Black beef cattle. BMC Res Notes 2:131. https://doi.org/10.1186/1756-0500-2-131

    Article  CAS  Google Scholar 

  78. Sukegawa S, Miyake T, Ibi T, Takahagi Y, Murakami H, Morimatsu F, Yamada T (2014) Multiple marker effects of single nucleotide polymorphisms in three genes, AKIRIN2, EDG1 and RPL27A, for marbling development in Japanese Black cattle. Anim Sci J 85(3):193–197. https://doi.org/10.1111/asj.12108

    Article  CAS  Google Scholar 

  79. Watanabe N, Satoh Y, Fujita T, Ohta T, Kose H, Muramatsu Y, Yamamoto T, Yamada T (2011) Distribution of allele frequencies at TTN g.231054C %3e T, RPL27A g.3109537C %3e T and AKIRIN2 c.*188G %3e A between Japanese Black and four other cattle breeds with differing historical selection for marbling. BMC Res Notes 4:10. https://doi.org/10.1186/1756-0500-4-10

    Article  CAS  Google Scholar 

  80. Jeong H, Song KD, Seo M, Caetano-Anolles K, Kim J, Kwak W, Oh JD, Kim E, Jeong DK, Cho S et al (2015) Exploring evidence of positive selection reveals genetic basis of meat quality traits in Berkshire pigs through whole genome sequencing. BMC Genet 16:104. https://doi.org/10.1186/s12863-015-0265-1

    Article  CAS  Google Scholar 

  81. Dong Y, Pan JS, Zhang L (2013) Myostatin suppression of Akirin1 mediates glucocorticoid-induced satellite cell dysfunction. PLoS ONE 8(3):e58554. https://doi.org/10.1371/journal.pone.0058554

    Article  CAS  Google Scholar 

  82. Mobley CB, Fox CD, Ferguson BS, Amin RH, Dalbo VJ, Baier S, Rathmacher JA, Wilson JM, Roberts MD (2014) L-leucine, beta-hydroxy-beta-methylbutyric acid (HMB) and creatine monohydrate prevent myostatin-induced Akirin-1/Mighty mRNA down-regulation and myotube atrophy. J Int Soc Sports Nutr 11:38. https://doi.org/10.1186/1550-2783-11-38

    Article  CAS  Google Scholar 

  83. Silva MT, Wensing LA, Brum PC, Camara NO, Miyabara EH (2014) Impaired structural and functional regeneration of skeletal muscles from beta2-adrenoceptor knockout mice. Acta Physiol (Oxford, England) 211(4):617–633. https://doi.org/10.1111/apha.12329

    Article  CAS  Google Scholar 

  84. Reichman R, Alleva B, Smolikove S (2017) Prophase I: preparing chromosomes for segregation in the developing oocyte. Results Probl Cell Differ 59:125–173. https://doi.org/10.1007/978-3-319-44820-6_5

    Article  CAS  Google Scholar 

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Acknowledgements

Work in the Weiner lab was supported by NIH Grant R01 NS055272 and by an Accelerator Grant from the Iowa Neuroscience Institute; work in the Smolikove lab was supported by NSF Grant 1515551.

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  1. Peter J. Bosch and Stacey L. Peek contributed equally to this article.

Authors and Affiliations

  1. Department of Biology and Iowa Neuroscience Institute, University of Iowa, 143 Biology Building, Iowa City, IA, 52242, USA

    Peter J. Bosch & Joshua A. Weiner

  2. Interdisciplinary Graduate Program in Neuroscience, Department of Biology and Iowa Neuroscience Institute, University of Iowa, 143 Biology Building, Iowa City, IA, 52242, USA

    Stacey L. Peek

  3. Department of Biology, University of Iowa, 143 Biology Building, Iowa City, IA, 52242, USA

    Sarit Smolikove

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  1. Peter J. Bosch
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  2. Stacey L. Peek
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  3. Sarit Smolikove
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  4. Joshua A. Weiner
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Contributions

PJB and JAW designed the article. PJB and SLP performed the research and wrote the manuscript. SS and JAW contributed to writing and editing and critically revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Joshua A. Weiner.

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Bosch, P.J., Peek, S.L., Smolikove, S. et al. Akirin proteins in development and disease: critical roles and mechanisms of action. Cell. Mol. Life Sci. 77, 4237–4254 (2020). https://doi.org/10.1007/s00018-020-03531-w

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  • DOI: https://doi.org/10.1007/s00018-020-03531-w

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