Skip to main content
Log in

Genomic loss of the HSP70cA gene in the vertebrate lineage

  • Short Communication
  • Published:
Cell Stress and Chaperones Aims and scope

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Irie N, Satoh N, Kuratani S (2018) The phylum Vertebrata: a case for zoological recognition. Zool Lett 4:1–20

    Article  Google Scholar 

  • Kaneko G (2022) Phylogenetic annotation of Drosophila melanogaster heat shock protein 70 genes. microPubl Biol 10:17912

    Google Scholar 

  • Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayer MP (2021) The Hsp70-chaperone machines in bacteria. Front Mol Biosci 8:512

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Potter I, Rothwell B (1970) The mitotic chromosomes of the lamprey, Petromyzon marinus L. Experientia 26:429–430

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shoguchi E et al (2004) Fluorescent in situ hybridization to ascidian chromosomes. Zool Sci 21:153–157

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the M.G. and Lillie A. Johnson Foundation, Victoria, TX, for supporting students involved in this research.

Funding

GK was supported by funding from M.G. and Lillie A. Johnson Foundation, Victoria, TX.

Author information

Authors and Affiliations

Authors

Contributions

Conceived and designed the experiments: HE, EY, and GK; performed experiments and data analyses: AM, BIR, MNR, DV, MMC, DOO, ELM, HJDLO, AMG, GGL, EY, and GK; contributed reagents/materials/analysis tools: HE and GK: wrote the paper: GK; read and approved the final manuscript: AM, BIR, MNR, DV, MMC, DOO, ELM, HJDLO, AMG, GGL, HE, EY, and GK.

Corresponding authors

Correspondence to Ermeng Yu or Gen Kaneko.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(XLSX 9 kb)

ESM 2

(XLSX 570 kb)

ESM 3

(XLSX 53 kb)

ESM 4

(XLSX 13 kb)

ESM 5

(PPTX 6172 kb)

ESM 6

(PPTX 53 kb)

ESM 7

(DOCX 70 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Merchant, A., Ramirez, B.I., Reyes, M.N. et al. Genomic loss of the HSP70cA gene in the vertebrate lineage. Cell Stress and Chaperones 28, 1053–1067 (2023). https://doi.org/10.1007/s12192-023-01370-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-023-01370-9

Keywords

Navigation