Abstract
In this article, we examine the evolution of Jak and Stat proteins, and of the Jak-Stat pathway. We first introduce the protein families involved and the signaling pathway in general. We then oppose the simply structured pathway in Drosophila melanogaster to the more complex situation in mammals. Furthermore, we compare the Jak-Stat system between mammals and teleost fishes. Finally, we move to the less well investigated roles of Stats in the worm Caenorhabditis elegans and the slime mold Dictyostelium discoideum. We also survey the distribution of Jaks and Stats among metazoans and other eukaryotes. Orthologs of Stats are widely distributed among metazoans and are also found in choanoflagellates and in slime molds. In contrast, Jaks seem to be confined to the bilaterians and are apparently absent in molluscs, round- and flatworms. This indicates that the Jak-Stat pathway evolved at the base of the bilaterians, but has been lost in some invertebrate groups.
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References
Araki T et al (1998) Developmentally and spatially regulated activation of a Dictyostelium STAT protein by a serpentine receptor. EMBO J 17(14):4018–4028
Arbouzova NI, Zeidler MP (2006) JAK/STAT signalling in Drosophila: insights into conserved regulatory and cellular functions. Development 133:2605–2616
Banninger G, Reich NC (2004) STAT2 nuclear trafficking. J Biol Chem 279:39199–39206
Chasman D et al (1999) Crystal structure of an OCA-B peptide bound to an Oct-1 POU domain/octamer DNA complex: specific recognition of a protein-DNA interface. Genes Dev 13(20):2650–2657
Chishti AH, Kim AC, Marfatia SM, Lutchman M, Hanspal M, Jindal H, Liu SC, Low PS, Rouleau GA, Mohandas N, Chasis JA, Conboy JG, Gascard P, Takakuwa Y, Huang SC, Benz EJ Jr, Bretscher A, Fehon RG, Gusella JF, Ramesh V, Solomon F, Marchesi VT, Tsukita S, Hoover KB et al (1998) The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem Sci 23:281–282
Decker T, Muller M, Stockinger S (2005) The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol 5:675–687
Dierking K, Polanowska J, Omi S, Engelmann I, Gut M, Lembo F, Ewbank JJ, Pujol N (2011) Unusual regulation of a STAT protein by an SLC6 family transporter in C. elegans epidermal innate immunity. Cell Host Microbe 9:425–435
Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sorensen MV, Haddock SH, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749
Ebersberger I, Strauss S, von Haeseler A (2009) HaMStR: profile hidden markov model based search for orthologs in ESTs. BMC Evol Biol 9:157
Gao Q, Hua J, Kimura R, Headd JJ, Fu XY, Chin YE (2004) Identification of the linker-SH2 domain of STAT as the origin of the SH2 domain using two-dimensional structural alignment. Mol Cell Proteomics 3:704–714
Gorissen M, de Vrieze E, Flik G, Huising MO (2011) STAT genes display differential evolutionary rates that correlate with their roles in the endocrine and immune system. J Endocrinol 209(2):175–184
Hino K, Satou Y, Yagi K, Satoh N (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis. VI. Genes for Wnt, TGFbeta, Hedgehog and JAK/STAT signaling pathways. Dev Genes Evol 213:264–272
Hughes AL, Friedman R (2003) 2R or not 2R: testing hypotheses of genome duplication in early vertebrates. J Struct Funct Genomics 3:85–93
Hughes AL, Friedman R (2004) Pattern of divergence of amino acid sequences encoded by paralogous genes in human and pufferfish. Mol Phylogenet Evol 32:337–343
Hunter T, Plowman GD (1997) The protein kinases of budding yeast: six score and more. Trends Biochem Sci 22:18–22
Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, De Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigo R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quetier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest CH (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957
Kawata T, Shevchenko A, Fukuzawa M, Jermyn KA, Totty NF, Zhukovskaya NV, Sterling AE, Mann M, Williams JG (1997) SH2 signaling in a lower eukaryote: a STAT protein that regulates stalk cell differentiation in dictyostelium. Cell 89:909–916
Kisseleva MV, Cao L, Majerus PW (2002) Phosphoinositide-specific inositol polyphosphate 5-phosphatase IV inhibits Akt/protein kinase B phosphorylation and leads to apoptotic cell death. J Biol Chem 277:6266–6272
Levy DE, Darnell JE Jr (2002) Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3:651–662
Meyer A, VdP Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27:937–945
Miyoshi K, Cui Y, Riedlinger G, Robinson P, Lehoczky J, Zon L, Oka T, Dewar K, Hennighausen L (2001) Structure of the mouse Stat 3/5 locus: evolution from Drosophila to zebrafish to mouse. Genomics 71:150–155
Na J, Tunggal B, Eichinger L (2007) STATc is a key regulator of the transcriptional response to hyperosmotic shock. BMC Genomics 8:123
O’Shea JJ, Gadina M, Schreiber RD (2002) Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 109(Suppl):S121–S131
Pesu M, Laurence A, Kishore N, Zwillich SH, Chan G, O’Shea JJ (2008) Therapeutic targeting of Janus kinases. Immunol Rev 223:132–142
Sackton TB, Lazzaro BP, Schlenke TA, Evans JD, Hultmark D, Clark AG (2007) Dynamic evolution of the innate immune system in Drosophila. Nat Genet 39:1461–1468
Schindler C, Shuai K, Prezioso VR, Darnell JE Jr (1992) Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257:809–813
Schindler C, Levy DE, Decker T (2007) JAK-STAT signaling: from interferons to cytokines. J Biol Chem 282:20059–20063
Sharman AC, Holland PWH (1996) Conservation, duplication and divergence of developmental genes during chordate evolution. Neth J Zool 46:47–67
Shuai K, Schindler C, Prezioso VR, Darnell JE Jr (1992) Activation of transcription by IFN-gamma: tyrosine phosphorylation of a 91-kD DNA binding protein. Science 258:1808–1812
Sidow A (1996) Gen(om)e duplications in the evolution of early vertebrates. Curr Opin Genet Dev 6:715–722
Van Valen L (1973) A new evolutionary law. Evol Theor 1:1–30
Vinkemeier U, Moarefi I, Darnell JE Jr, Kuriyan J (1998) Structure of the amino-terminal protein interaction domain of STAT-4. Science 279:1048–1052
Wang Y, Levy DE (2006) C. elegans STAT: evolution of a regulatory switch. FASEB J 20:1641–1652
Wang X, Watt PM, Louis EJ, Borts RH, Hickson ID (1996) Pat1: a topoisomerase II-associated protein required for faithful chromosome transmission in Saccharomyces cerevisiae. Nucleic Acids Res 24:4791–4797
Weiler S, Mou S, DeBerry CS, Keller JR, Ruscetti F, Ferris DK, Longo DL, Linnekin D (2011) JAK2 is associated with the c-kit proto-oncogene product and is phosphorylated in response to stem cell factor. Blood 87:3688–3693
Wittbrodt JMA, Schartl M (1998) More genes in fish? Bioessays 20:511–515
Wojciak JM et al (2009) Structural basis for recruitment of CBP/p300 coactivators by STAT1 and STAT2 transactivation domains. EMBO J 28(7):948–958
Yao Z, Cui Y, Watford WT, Bream JH, Yamaoka K, Hissong BD, Li D, Durum SK, Jiang Q, Bhandoola A, Hennighausen L, O’Shea JJ (2006) Stat5a/b are essential for normal lymphoid development and differentiation. Proc Natl Acad Sci USA 103:1000–1005
Zhukovskaya NV et al (2004) Dd-STATb, a Dictyostelium STAT protein with a highly aberrant SH2 domain, functions as a regulator of gene expression during growth and early development. Development 131(2):447–458
Acknowledgments
We would like to thank Mathias Müller, Thomas Decker, and Birgit Strobl for critically reading the manuscript and Nicole Leitner and again Birgit Strobl for help during various stages of the manuscript. The research of CV is supported by and PS is funded by the FWF SFB-F28. IE acknowledges funding by the Wiener Wissenschafts-, Forschungs- und Technologie Fonds (WWTF), and from the DFG priority program SPP 1174 Deep Metazoan Phylogeny [Grant HA 1628/9].
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Vogl, C., Shukla, P., Ebersberger, I. (2012). Evolution of Jak and Stat Proteins. In: Decker, T., Müller, M. (eds) Jak-Stat Signaling : From Basics to Disease. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0891-8_7
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DOI: https://doi.org/10.1007/978-3-7091-0891-8_7
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