Genomic loss of the HSP70cA gene in the vertebrate lineage.
Chordata
Comparative genomics
Heat shock protein
Molecular evolution
Synteny
Journal
Cell stress & chaperones
ISSN: 1466-1268
Titre abrégé: Cell Stress Chaperones
Pays: Netherlands
ID NLM: 9610925
Informations de publication
Date de publication:
17 Aug 2023
17 Aug 2023
Historique:
received:
12
12
2022
accepted:
08
08
2023
revised:
07
08
2023
medline:
17
8
2023
pubmed:
17
8
2023
entrez:
16
8
2023
Statut:
aheadofprint
Résumé
Metazoan 70 kDa heat shock protein (HSP70) genes have been classified into four lineages: cytosolic A (HSP70cA), cytosolic B (HSP70cB), endoplasmic reticulum (HSP70er), and mitochondria (HSP70m). Because previous studies have identified no HSP70cA genes in vertebrates, we hypothesized that this gene was lost on the evolutionary path to vertebrates. To test this hypothesis, the present study conducted a comprehensive database search followed by phylogenetic and synteny analyses. HSP70cA genes were found in invertebrates and in two of the three subphyla of Chordata, Cephalochordata (lancelets) and Tunicata (tunicates). However, no HSP70cA gene was found in the genomes of Craniata (another subphylum of Chordata; lamprey, hagfish, elephant shark, and coelacanth), suggesting the loss of the HSP70cA gene in the early period of vertebrate evolution. Synteny analysis using available genomic resources indicated that the synteny around the HSP70 genes was generally conserved between tunicates but was largely different between tunicates and lamprey. These results suggest the presence of dynamic chromosomal rearrangement in early vertebrates that possibly caused the loss of the HSP70cA gene in the vertebrate lineage.
Identifiants
pubmed: 37587350
doi: 10.1007/s12192-023-01370-9
pii: 10.1007/s12192-023-01370-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s), under exclusive licence to Cell Stress Society International.
Références
Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165
Drosopoulou E, Chrysopoulou A, Nikita V, Mavragani-Tsipidou P (2009) The heat shock 70 genes of the olive pest Bactrocera oleae: genomic organization and molecular characterization of a transcription unit and its proximal promoter region. Genome 52:210–214
doi: 10.1139/G08-110
pubmed: 19234568
Grewal SH, Yoshinaga T, Ehsan H, Yu E, Kaneko G (2023) A genome-wide screening of the 70 kDa heat shock protein (HSP70) genes in the rotifer Brachionus plicatilis sensu stricto with a characterization of two heat-inducible HSP70 genes. Cell Stress Chaperones, published online. https://doi.org/10.1007/s12192-022-01260-6
Hasnain P, Kaneko G (2022) Phylogenetic annotation of Caenorhabditis elegans heat shock protein 70 genes. microPubl Biol 10:000633
Huang X, Li S, Gao Y, Zhan A (2018) Genome-wide identification, characterization and expression analyses of heat shock protein-related genes in a highly invasive ascidian Ciona savignyi. Front Physiol 9:1043
doi: 10.3389/fphys.2018.01043
pubmed: 30108524
pmcid: 6079275
Irie N, Satoh N, Kuratani S (2018) The phylum Vertebrata: a case for zoological recognition. Zool Lett 4:1–20
doi: 10.1186/s40851-018-0114-y
Kaneko G (2022) Phylogenetic annotation of Drosophila melanogaster heat shock protein 70 genes. microPubl Biol 10:17912
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166
doi: 10.1093/bib/bbx108
pubmed: 28968734
Kourtidis A, Drosopoulou E, Nikolaidis N, Hatzi VI, Chintiroglou CC, Scouras ZG (2006) Identification of several cytoplasmic HSP70 genes from the Mediterranean mussel (Mytilus galloprovincialis) and their long-term evolution in Mollusca and Metazoa. J Mol Evol 62:446–459. https://doi.org/10.1007/s00239-005-0121-4
doi: 10.1007/s00239-005-0121-4
pubmed: 16547643
Krysiak K, Tibbitts JF, Shao J, Liu T, Ndonwi M, Walter MJ (2015) Reduced levels of Hspa9 attenuate Stat5 activation in mouse B cells. Exp Hematol 43:319–330
doi: 10.1016/j.exphem.2014.12.005
pubmed: 25550197
Kuraku S, Zmasek CM, Nishimura O, Katoh K (2013) aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res 41:W22–W28
doi: 10.1093/nar/gkt389
pubmed: 23677614
pmcid: 3692103
Liu D et al (2022) Genome-wide analyses of heat shock protein superfamily provide new insights on adaptation to sulfide-rich environments in Urechis unicinctus (Annelida, Echiura). Int J Mol Sci 23:2715
doi: 10.3390/ijms23052715
pubmed: 35269857
pmcid: 8910992
Mattos DR et al (2022) Canine osteosarcoma cells exhibit basal accumulation of multiple chaperone proteins and are sensitive to small molecule inhibitors of GRP78 and heat shock protein function. Cell Stress Chaperones 27:223–239
doi: 10.1007/s12192-022-01263-3
pubmed: 35244890
pmcid: 9106791
Mayer MP (2021) The Hsp70-chaperone machines in bacteria. Front Mol Biosci 8:512
doi: 10.3389/fmolb.2021.694012
Mohamad MI, Desoky IA, Zaki KA, Sadek DR, Kassim SK, Mohamed DA-W (2022) Pterostilbene ameliorates the disrupted Adars expression and improves liver fibrosis in DEN-induced liver injury in Wistar rats: A novel potential effect. Gene 813:146124
doi: 10.1016/j.gene.2021.146124
pubmed: 34921950
Potter I, Rothwell B (1970) The mitotic chromosomes of the lamprey, Petromyzon marinus L. Experientia 26:429–430
doi: 10.1007/BF01896930
pubmed: 5439626
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard, MA, Huelsenbeck JP (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
Satoh N, Rokhsar D, Nishikawa T (2014) Chordate evolution and the three-phylum system. Proc R Soc Lond Ser B Biol Sci 281:20141729
Schnebert S, Goguet M, Vélez EJ, Depincé A, Beaumatin F, Herpin A, Seiliez I (2022) Diving into the evolutionary history of HSC70-linked selective autophagy pathways: endosomal microautophagy and chaperone-mediated autophagy. Cells 11:1945
doi: 10.3390/cells11121945
pubmed: 35741074
pmcid: 9221867
Shoguchi E et al (2004) Fluorescent in situ hybridization to ascidian chromosomes. Zool Sci 21:153–157
doi: 10.2108/zsj.21.153
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539
Velazquez JM, Lindquist S (1984) hsp70: nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell 36:655–662
doi: 10.1016/0092-8674(84)90345-3
pubmed: 6421488
Wada S, Hamada M, Satoh N (2006) A genomewide analysis of genes for the heat shock protein 70 chaperone system in the ascidian Ciona intestinalis. Cell Stress Chaperones 11:23–33
doi: 10.1379/CSC-137R.1
pubmed: 16572726
pmcid: 1400611
Wallace IM, O’sullivan O, Higgins DG, Notredame C (2006) M-Coffee: combining multiple sequence alignment methods with TCoffee. Nucleic Acids Res 34:1692–1699
Wright ES (2016) Using DECIPHER v2. 0 to analyze big biological sequence data in R. R Journal 8:352–359
doi: 10.32614/RJ-2016-025
Yu E, Yoshinaga T, Jalufka F, Ehsan H, Mark Welch DB, Kaneko G (2021) The complex evolution of the metazoan HSP70 gene family. Sci Rep 11:17794. https://doi.org/10.1038/s41598-021-97192-9
doi: 10.1038/s41598-021-97192-9
pubmed: 34493758
pmcid: 8423806