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Entry PTX4 Evolution of the Pentraxin Family Evolution of the Pentraxin Family: The New Entry PTX4 Yeny Martinez de la Torre, Marco Fabbri, Sebastien Jaillon, Antonio Bastone, Manuela Nebuloni, Annunciata Vecchi, This information is current as Alberto Mantovani and Cecilia Garlanda of September 24, 2021. J Immunol published online 31 March 2010 http://www.jimmunol.org/content/early/2010/03/31/jimmun ol.0901672 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2010/03/31/jimmunol.090167 Material 2.DC1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 24, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Published March 31, 2010, doi:10.4049/jimmunol.0901672 The Journal of Immunology Evolution of the Pentraxin Family: The New Entry PTX4 Yeny Martinez de la Torre,* Marco Fabbri,* Sebastien Jaillon,* Antonio Bastone,† Manuela Nebuloni,‡ Annunciata Vecchi,* Alberto Mantovani,*,x and Cecilia Garlanda* Pentraxins (PTXs) are a superfamily of multifunctional conserved proteins, some of which are components of the humoral arm of innate immunity and behave as functional ancestors of Abs. They are divided into short (C-reactive protein and serum amyloid P component) and long pentraxins (PTX3 and neuronal pentraxins). Based on a search for pentraxin domain-containing sequences in databases, a phylogenetic analysis of the pentraxin family from mammals to arthropods was conducted. This effort resulted in the identification of a new long pentraxin (PTX4) conserved from mammals to lower vertebrates, which clusters alone in phylogenetic analysis. The results indicated that the pentraxins consist of five clusters: short pentraxins, which can be found in chordate and arthropods; neuronal pentraxins; the prototypic long pentraxin PTX3, which originated very early at the divergence of the verte- brates; the Drosophila pentraxin-like protein B6; and the long pentraxin PTX4 discovered in this study. Conservation of flanking genes in mammalian evolution indicates maintenance of synteny. Analysis of PTX4, in silico and by transcript expression, shows Downloaded from that the gene is well conserved from mammals to lower vertebrates and has a unique pattern of mRNA expression. Thus, PTX4 is a new unique member of the pentraxin superfamily, conserved in evolution. The Journal of Immunology, 2010, 184: 000–000. entraxins (PTXs) are a superfamily of multifunctional that regulate innate resistance to microbes and the scavenging of conserved proteins that are characterized by a cyclic cellular debris, conserved from mammals to arthropods (1). In P multimeric structure and by the presence in their carboxyl- Limulus polyphemus, different forms of CRPs and SAP are normal http://www.jimmunol.org/ terminal of an ∼200 aa-long conserved domain, called pentraxin and abundant constituents of the hemolymph and are involved in domain. In addition, all the members of this family share an 8 aa- recognizing and destroying pathogens (3–5). long conserved sequence (HxCxS/TWxS, in which x is any amino PTX3 and subsequently other long pentraxins were identified in acid) in the pentraxin domain, called pentraxin signature (1). the 1990s as inducible genes or molecules expressed in specific Some pentraxins, together with collectins and ficolins, constitute tissues (e.g., neurons, spermatozoa) (6–8). Long pentraxins have the humoral arm of innate immunity and behave as functional an unrelated, long amino-terminal domain coupled to the car- ancestors of Abs by mediating agglutination, complement acti- boxyl-terminal pentraxin domain and differ, with respect to short vation, and opsonisation (2). pentraxins, in their gene organization, chromosomal localization, by guest on September 24, 2021 C-reactive protein (CRP), which, together with serum amyloid P cellular source, and in inducing stimuli and ligand-recognition (SAP) component (APCS), constitutes the short pentraxin arm of ability. In particular, PTX3 behaves as a soluble pattern recogni- the superfamily, was the first fluid-phase pattern recognition tion receptor playing a nonredundant role in innate immunity molecule to be identified and named after its ability to bind in against selected pathogens (9–11); it also has a nonredundant role a calcium-dependent manner the C-polysaccharide of Strepto- in female fertility due to its structural role in the extracellular coccus pneumoniae (2). CRP and SAP are acute-phase proteins matrix (12, 13). PTX3 has also been observed to have a regulatory role on inflammation by acting as a feedback mechanism of in- hibition of leukocyte recruitment (14). *Laboratorio di Immunologia e Infiammazione, Istituto Clinico Humanitas, Istituto The long pentraxins identified after PTX3 include guinea pig † Di Ricovero e Cura a Carattere Scientifico, Rozzano; Mario Negri Institute for apexin (15, 16), neuronal pentraxin (NP or NPTX) 1 (17, 18) and Pharmacological Research; and ‡Pathology Unit, L. Sacco Department of Clinical Sciences and xDepartment of Translational Medicine, University of Milan, Milan, NP2, also called NPTX2 or NARP (19, 20), and NPTX receptor, Italy which is the only member associated to the cell through a trans- Received for publication May 27, 2009. Accepted for publication March 3, 2010. membrane domain (21–23) (see below). NPTXs have been shown This work was supported by Associazione Italiana per la Ricerca sul Cancro, Min- to be involved in the excitatory synaptic remodeling (21). NPTX2 istero Istruzione Universita` e Ricerca (RBLA039LSF_007), European Commission has been implicated in long-term neuronal plasticity as well as (project MUGEN, LSHG-CT-2005-005203), Cariplo (Project Nobel), and European Research Council (project HIIS). dopaminergic nerve cell death (24) and NPTX1 in hypoxia-is- chemia– and amyloid-b–induced neuronal death (25, 26). The name PTX4 was approved by the HUGO Gene Nomenclature Committee on March 25, 2010. The pentraxin domain has also been found in multidomain Address correspondence and reprint requests to Dr. Alberto Mantovani and Dr. Cecilia proteins, such as in the extracellular protein polydom [which Garlanda, Istituto Clinico Humanitas, Via Manzoni 113, I-20089, Rozzano, Milan, Italy. includes an N-terminal von Willebrand factor A domain, 2 hyalin E-mail addresses: [email protected] and cecilia.garlanda@ repeat domains, 10 epidermal growth factor repeats, 34 comple- humanitasresearch.it ment control protein domains, and a single pentraxin domain (27)] The online version of this article contains supplemental material. and in a few adhesion G-protein–coupled receptors (GPRs), in Abbreviations used in this paper: C, pentraxin domain; CRP, C-reactive protein; EMBL, European Molecular Biology Laboratory; FP, female protein; GPR, G-protein–coupled particular GPR144, GPR112, and GPR126 (28) (Simple Modular receptor; Mptx, mucosal pentraxin; MS, mass spectrometry; N, N-terminal domain; Architecture Research Tool, http://smart.embl-heidelberg.de/; NCBI, National Center for Biotechnology Information; NJ, neighbor-joining; NP or Prosite, www.expasy.org/prosite/database). The function of these NPTX, neuronal pentraxin; PTX, pentraxin; SAP, serum amyloid P. proteins has not been defined yet, nor has the role of the pentraxin Copyright Ó 2010 by The American Association of Immunologists, Inc. 0022-1767/10/$16.00 domain in multidomain proteins. www.jimmunol.org/cgi/doi/10.4049/jimmunol.0901672 2 THE NEW PENTRAXIN PTX4 The present study was designed as a search for pentraxin do- Quantitative real-time PCR main-containing sequences in different databases. We found that Tissues were homogenized, and total RNA was extracted by TRIzol based on phylogenetic analysis, the pentraxin superfamily consists (Invitrogen, Carlsbad, CA). cDNA was synthesized from 1 mg total RNA of five distinct clusters. This effort led to the identification of a new after DNase treatment by High Capacity cDNA archive kit (Applied long pentraxin (PTX4) conserved from mammals to lower verte- Biosystems). The following primers were designed with Primer Express brates, which clusters alone in phylogenetic analysis. software (Applied Biosystems): mouse pentraxin (mPTX)3 (sense, 59-ACGAAATAGACAATGGACTTCATCC-39, antisense, 59-AGTCG- CATGGCGTGGG-39); mPTX4 (sense, 59-TCATCAAGCAGCCCCACC- Materials and Methods 39, antisense, 59-TTGCAAATGTTTCCTGGTCCT-39); b-actin (sense, 59- Bioinformatics TCACCCACACTGTGCCCATCTACGA-39,antisense,59-CAGCGGAACC- GCTCATTGCCAATGG-39); hPTX3 (sense, 59-CGAAATAGACAATGG- Sequences were retrieved from the Swiss-prot (www.ebi.ac.uk/swissprot/), ACTCCATCC-39, antisense, 59-CAGGCGCACGGCGT-39); and hPTX4 National Center for Biotechnology Information (NCBI) (http://ncbi.nlm. (sense, 59-TCCGGAGATTCCAGGAGGT-39,antisense,59-TGCTGGCGAT- nih.gov), European Molecular Biology Laboratory (EMBL; www.ebi.ac. GTTCTGCA-39). Quantitative real-time PCR was performed using the Sybr uk/embl/),
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