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Ancient Cytokines, the Role of Astakines As Hematopoietic Growth Factors*DS http://www.diva-portal.org This is the published version of a paper published in Journal of Biological Chemistry. Citation for the original published paper (version of record): Lin, X., Novotny, M., Söderhäll, K., Söderhäll, I. (2010) Ancient Cytokines, the Role of Astakines as Hematopoietic Growth Factors Journal of Biological Chemistry, 285(37): 28577-28586 https://doi.org/10.1074/jbc.M110.138560 Access to the published version may require subscription. N.B. When citing this work, cite the original published paper. Copyright The American Society for Biochemistry and Molecular Biology Permanent link to this version: http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-135009 THE JOURNAL OF BIOLOGICAL CHEMISTRY VOL. 285, NO. 37, pp. 28577–28586, September 10, 2010 © 2010 by The American Society for Biochemistry and Molecular Biology, Inc. Printed in the U.S.A. Ancient Cytokines, the Role of Astakines as Hematopoietic Growth Factors*□S Received for publication, April 27, 2010, and in revised form, June 18, 2010 Published, JBC Papers in Press, June 30, 2010, DOI 10.1074/jbc.M110.138560 Xionghui Lin‡, Marian Novotny§1, Kenneth So¨derha¨ll‡, and Irene So¨derha¨ll‡2 From the ‡Department of Comparative Physiology, Uppsala University, Norbyva¨gen 18A, 752 36 Uppsala, Sweden and the §Department of Cell Biology, Faculty of Sciences, Charles University in Prague, Vinicna 7, Praha 12843, Czech Republic Hematopoiesis is the process by which hemocytes mature and hemocytes: semigranular cells (SGC), and granular cells (GC) subsequently enter the circulation. Vertebrate prokineticins (3). The molecular mechanism by which Hpt cells are induced (PKs) are known to take part in this process, as are the inverte- to proliferate and differentiate into hemocytes is starting to brate prokineticin domain proteins, astakines. In Pacifastacus be understood in some invertebrates, including crustaceans. leniusculus, astakine 1 is essential for the release of new hemo- Recently, a cytokine, astakine, has been shown to be important cytes into the open circulatory system of these animals. In addi- in this process (2–6). Astakine, a homologue to vertebrate pro- Downloaded from tion to astakine 1, we have now cloned a homologue of astakine kineticins, was first identified in Pacifastacus leniusculus and 1 with an insert of 13 amino acids, named as astakine 2. Both was found to be necessary for new hemocyte synthesis and crustacean astakines lack the N-terminal AVIT motif, which is release (3). present in vertebrate PKs, and hence receptor binding differs In vivo, when crayfish was injected with either native or from that of vertebrate PKs. We have found astakine-like recombinant astakine, the total hemocyte number was signifi- http://www.jbc.org/ sequences in 19 different invertebrate species, and the cantly increased, and astakine RNAi resulted in low hemocyte sequences show that some motifs are conserved among inver- recovery after LPS stimulation. In vitro, when a primary cell tebrate groups. Previously we showed that astakine 1 is culture of crayfish Hpt cells was incubated with astakine, pro- directly involved in hematopoiesis, and now we show that liferation was stimulated. Moreover, the addition of astakine astakine 1 and astakine 2 have different roles in hemocyte results in a decrease of activity of an extracellular transglutami- at Uppsala Universitetsbibliotek on August 19, 2019 lineage differentiation. Astakine 1 can stimulate prolifera- nase (TGase). This loss of TGase activity enables migration of tion of hematopoietic tissue (Hpt) cells (precursor of hemo- the cells out of the hematopoietic tissue (4). Furthermore, we cytes) as well as specifically induce differentiation of Hpt cells also showed that ATP synthase is present on the surface of a along the semigranular cell lineage, whereas astakine 2 plays subpopulation of the Hpt cells and that it serves as a receptor a role in granular cell differentiation. Moreover, we discuss for astakine. Surface ATP synthase activity contributes to about the impact of the putative structures of different astakines in 40% of the extracellular ATP formation on the surface of the comparison with the vertebrate prokineticins. Hpt cells, and astakine was found to interact with the ␤-subunit of ATP synthase, which resulted in a block of the ATP forma- tion by this enzyme (5). Crustaceans, as other invertebrates, rely on innate immunity The molecular mechanism of hematopoiesis in invertebrates for the protection of the animal against invading microorgan- has been mainly studied in Drosophila melanogaster and P. le- isms. The circulating hemocytes are crucial in these processes niusculus. Several transcription factors have been character- by participating in recognition, phagocytosis, melanization, ized as lineage-specific markers in the fruit fly, and they are and cytotoxicity (1). Thus, the regulation of hemocyte number conserved across taxonomic groups from flies to mammals is critical for the health of the animal, and the continuous for- (7–9). Accordingly, the importance of GATA transcription fac- mation of new hemocytes (hematopoiesis) is tightly regulated tors as well as a Runt protein homologue during hematopoiesis by factors released from circulating hemocytes (2). In crayfish, has been shown in P. leniusculus (4). The importance of differ- the hematopoietic tissue (Hpt)3 is a separate organ, containing ent signaling pathways, such as Toll/NF-␬B, and JAK/STAT five distinct types of Hpt cells, developing into two lineages of during embryonic and larval hematopoiesis has been studied in detail in Drosophila (9). A clear role for cytokines, such as the PDGF/VEGF-related PVF1-PVF3 and Upd (a ligand for the * This work was supported by the Swedish Science Research Council and the JAK/STAT pathway), in Drosophila hematopoiesis needs fur- Swedish Research Council Formas. □S The on-line version of this article (available at http://www.jbc.org) contains ther detailed studies (10, 11). Interestingly, no astakine or pro- supplemental Fig. 1. kineticin homologue is present in the genome of Drosophila or 1 Supported by Research Project LC 07032 of the Czech Ministry of Education, other dipterans, although such sequences are present in some Youth, and Sports. other insect orders, as well as in several other arthropods. 2 To whom correspondence should be addressed. Tel.: 46-18-4712817; Fax: 46-18-4716425; E-mail: [email protected]. Recently, specific marker proteins for Hpt cells, SGC, and GC 3 The abbreviations used are: Hpt, hematopoietic tissue; SGC, semigranular were identified in P. leniusculus (6). One specific Kazal protein- cell(s); GC, granular cell(s); KPI, Kazal proteinase inhibitor; SOD, superoxide ase inhibitor (KPI) was found to be exclusively expressed in dismutase; PCNA, proliferating cell nuclear antigen; RACE, rapid amplifica- tion of cDNA ends; Trx, thioredoxin; r-astakine, recombinant astakine; SGC, a superoxide dismutase (SOD) is transcribed only in GC, TGase, transglutaminase. and a proliferating cell nuclear antigen (PCNA) is only ex- SEPTEMBER 10, 2010•VOLUME 285•NUMBER 37 JOURNAL OF BIOLOGICAL CHEMISTRY 28577 Ancient Cytokines pressed in proliferating cells and was accordingly detected in induced with 0.02 ␮M isopropyl 1-thio-␤-D-galactopyranoside P. leniusculus Hpt cells. Because crayfish hemocytes do not overnight at 20 °C. The recombinant protein was purified by divide in the circulatory system, this transcript can serve as a HisTrap FF column chromatography (GE Healthcare), and the good marker for Hpt cells. These three marker proteins make it thioredoxin (Trx) tag combined with S tag and His tag was possible for us to study the mechanism by which astakine removed in the column by incubation with enterokinase (New affects hematopoiesis in P. leniusculus. Therefore, P. leniuscu- England Biolabs) at 4 °C in cleavage buffer (20 mM Tris-HCl, 50 lus is a good model to study the role of these cytokines in blood mM NaCl, 2 mM CaCl2, pH 7.2) overnight. Free astakine 1 was cell development in invertebrates. In the current study, we pro- eluted with elution buffer (20 mM Tris-HCl, 50 mM NaCl, 5 mM vide direct evidence from in vitro Hpt cell culture and in vivo EDTA, pH 7.2) from the column, and the enterokinase was experiments for different functions of two related astakines irreversibly blocked by 4 mM Pefabloc SC (Roche Applied during hematopoiesis. Science). For astakine 2, the coding region without signal peptide was EXPERIMENTAL PROCEDURES cloned into the same vector at the EcoRI and SalI cleavage sites, Experimental Animals—Freshwater crayfish, P. leniusculus, and furthermore one Factor Xa site was introduced in the N purchased from Nils Fors (Askersund, Lake Va¨ttern, Sweden) terminus. Thus, the tag of recombinant astakine 2 was removed were maintained in tanks with aerated tap water at 10 °C. Only on the column by incubation with Factor Xa, which generates Downloaded from intermolt animals were used in the experiment. an identical N-terminal in the recombinant astakine 2 as in Molecular Cloning of Astakine 2—For cDNA cloning, nested native astakine 2. Factor Xa activity was irreversibly blocked by degenerate primers were designed according to the amino acid 2 ␮M dansyl-Glu-Gly-Arg-chloromethyl ketone (catalog no. sequence GMCPCR (5Ј-ICK RCA IGG RCA CAT ICC-3Ј) and 251700, Calbiochem). TCQLP (5Ј-IGG IAR YTG RCA IGT-3Ј) that are the homo- Expression of Astakine in Spodoptera frugiperda (Sf9) Cells— logue region in P. leniusculus astakine (hereafter named The cDNA encoding the astakine
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