High-Mobility-Group family genes from Lampetra japonica reveal their early origin and molecular evolution in the vertebrate lineage

다국어 초록 (Multilingual Abstract)

High-mobility group family (HMG) genes are ubiquitous in vertebrates, including mammals, birds, amphibians and fishes.
To elucidate the molecular phylogeny of the HMG genes in the primitive vertebrate, we have cloned three homologues of HMG-box genes, called Lj-HMGB1, Lj-HMGB2 and Lj-HMGBX, from a cDNA library generated from lymphocyte-like cells of the Japanese lamprey (Lampetra japonica),an Agnathan that occupies a critical phylogenetic position between invertebrates and vertebrates. The open reading frames of Lj-HMGB1, Lj-HMGB2 and Lj-HMGBX contained 627 bp,585 bp and 678 bp, respectively. The analysis of the deduced amino acid sequences indicated that these three putative Lj-HMGB proteins contain four domains: HMG-box A,HMG-box B, an acidic carboxyl-terminal tail and a linker. A phylogenetic analysis revealed that the Lj-HMGB proteins fall outside the vertebrate clade; Lj-HMGBX is descended from a gene ancestral to the mammalian HMGB1/2/3. This discovery implies that there was a gene duplication event in the HMGB1/2/3 gene family that occurred after the divergence of the vertebrates (Cyclostomata) from the Cephalochordata and Urochordata at least 450 million years ago (MYA). The Lj-HMGB1, Lj-HMGB2 and Lj-HMGBX genes were detected in most tissues of the lamprey by RT-PCR. Our findings provide insight into the phylogeny of the HMGB genes in vertebrates.

참고문헌 (Reference)

1 Ardoin SP, "The role of cell death in the pathogenesisof autoimmune disease: HMGB1 and microparticles asintercellular mediators of inflammation" 18 : 319-326, 2008

2 Pedersen DS, "The plant-specificfamily of DNA-binding proteins containing three HMG-boxdomains interacts with mitotic and meiotic chromosomes" 192 : 577-589, 2011

3 Mitkova E, "The inhibitoryeffect of HMGB-1 protein on the repair of cisplatin-damagedDNA is accomplished through the acidic domain" 44 : 5893-5898, 2005

4 Degryse B, "The high mobility group(HMG) boxes of the nuclear protein HMG1 induce chemotaxisand cytoskeleton reorganization in rat smooth muscle cells" 152 : 1197-1206, 2001

5 Lee KB, "The effect of the acidic tail on theDNA-binding properties of the HMG1, 2 class of proteins: insightsfrom tail switching and tail Removal" 304 : 135-149, 2000

6 Müller S, "The double life of HMGB1chromatin protein: architectural factor and extracellular signal" 20 : 4337-4340, 2001

7 Zhang N, "The construction of Leukocyte cDNA library and bioinformaticsanalysis of Lampetra japonica" 33 : 237-241, 2010

8 Baxevanis BD, "The HMG-1 box protein family:classification and functional relationships" 23 : 1604-1613, 1995

9 Thompson JD, "The ClustalX Windows interface: Flexible strategiesfor multiple sequence alignment aided by quality analysis tools" 24 : 4876-4882, 1997

10 Li J, "Structural basisfor the proinflammatory cytokine activity of high mobility groupbox 1" 9 : 37-45, 2003

11 Vangent DC, "Stimulation ofV(D)J cleavage by high mobility group proteins" 16 : 2665-2670, 1997

12 Bustin M, "Revised nomenclature for high mobility group(HMG) chromosomal proteins" 26 : 152-153, 2001

13 Scaffidi P, "Release of chromatin protein HMGB1 by necrotic cells triggers inflammation" 418 : 191-195, 2002

14 Muller S, "Regulated expressionand subcellular localization of HMGB1, a chromatin protein witha cytokine function" 255 : 332-343, 2004

15 Ronfani L, "Reduced fertility and spermatogenesisdefects in mice lacking chromosomal protein Hmgb2" 128 : 1265-1273, 2001

16 Niemeyer CC, "Purificationof a high-mobility-group 1 sea-urchin protein and cloning ofcDNAs" 164 : 211-218, 1995

17 Ugrinova I, "NativeHMGB1 protein inhibits repair of cisplatin-damaged nucleosomesin vitro" 41 : 1556-1562, 2009

18 Bonaldi T, "Monocytic cellshyperacetylate chromatin protein HMGB1 to redirect it towardssecretion" 22 : 5551-5560, 2003

19 Kumar S, "MEGA3: Integrated softwarefor molecular evolutionary genetics analysis and sequencealignment" 5 : 150-163, 2004

20 Ishii A, "Lamprey TLRs with properties distinct from thoseof the variable lymphocyte receptors" 178 : 397-406, 2007

21 Pang Yue, "Identificationand characterization of the lamprey high-mobility group box 1gene" 7 : e35755-, 2012

22 Sower SA, "Identification of sea lamprey GTH [beta]-like cDNA and itsevolutionary implications" 148 : 22-32, 2006

23 Nemeth MJ, "Hmgb3: an HMG-box family memberexpressed in primitive hematopoietic cells that inhibits myeloidand B-cell differentiation" 102 : 1298-1306, 2003

24 Lotze MT, "High-mobility group box 1 protein(HMGB1): nuclear weapon in the immune arsenal" 5 : 331-342, 2005

25 Tang D, "HMGB1, OxidativeStress, and Disease" 10 : 1275-1312, 2010

26 Agresti A, "HMGB proteins and geneexpression" 13 : 170-178, 2003

27 O'Connor KA, "Further characterization of high mobilitygroup box 1(HMGB1) as a proinflammatory cytokine: centralnervous system effects" 24 : 254-265, 2003

28 Bianchi ME, "Flexing DNA: HMG-box proteinsand their partners" 63 : 1573-1577, 1998

29 Gao Q, "Expressed sequencetags (ests) analysis of the oral gland of Lampetra japonica" 32 : 1045-1052, 2005

30 Amemiya CT, "Evolution and developmentof immunological structures in the lamprey" 19 : 535-541, 2007

31 Zhu LN, "ESTs analyses of Lampetrajaponica liver and comparation transcriptome with the jawedvertebrates" 1 : 27-37, 2008

32 Doolittle RF, "Determining divergence times of the major kingdoms of livingorganisms with a protein clock" 271 : 470-477, 1996

33 Sharman AC, "Cloning andanalysis of an HMG gene from the lamprey Lampetra fluviatilis:gene duplication in vertebrate evolution" 184 : 99-105, 1997

34 Lehming N, "An HMG-like protein that can switch a transcriptionalactivator to a repressor" 371 : 175-179, 1994

35 Goodwin GH, "A new group of chromatin-associated proteins with a high content of acidic and basicamino acids" 38 : 14-19, 1973