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PreprintCited by 34Proteoglycans and glycosaminoglycans researchSubterranean biodiversity and taxonomyTardigrade Biology and Ecology

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Evolution of High-Molecular-Mass Hyaluronic Acid is Associated with Subterranean Lifestyle

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Zhao, Yang, Zheng, Zhizhong, Zhang, Zhihui, Hillpot, Eric, Lin, Yifei S., Zakusilo, Frances T., Lu, J. Yuyang, Ablaeva, Julia, Miller, Richard A., Nevo, Eviatar, Seluanov, Andrei, Gorbunova, Vera·2023·Nature Communications
DOI 10.1101/2023.05.08.539764PMC PMC10698142

Preprint — published as 10.1038/s41467-023-43623-2 · Paper page

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Abstract

Hyaluronic acid (HA) is a major component of extracellular matrix (ECM) which plays an important role in development, cellular response to injury and inflammation, cell migration, and cancer. The naked mole-rat (NMR, Heterocephalus glaber ) contains abundant high-molecular-mass HA (HMM-HA) in its tissues, which contributes to this species’ cancer resistance and possibly longevity. Here we report that abundant HMM-HA is found in a wide range of subterranean mammalian species, but not in phylogenetically related aboveground species. These species accumulate abundant HMM-HA by regulating the expression of genes involved in HA degradation and synthesis and contain unique mutations in these genes. The abundant high molecular weight HA may benefit the adaptation to subterranean environment by increasing skin elasticity and protecting from oxidative stress due to hypoxic subterranean environment. HMM-HA may also be coopted to confer cancer resistance and longevity to subterranean mammals. Our work suggests that HMM-HA has evolved with subterranean lifestyle.

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Research works printed but not linked: 83

  1. 10.1038/nature12234 · DOI
  2. 10.1073/pnas.1217211109 · DOI
  3. 2018, Limited Evidence for Parallel Molecular Adaptations Associated with the Subterranean Niche in Mammals: A Comparative Study of Three Superorders, Molecular biology and evolution, 35, 2544, 10.1093/molbev/msy161 · DOI
  4. 2014, Adaptations to a subterranean environment and longevity revealed by the analysis of mole rat genomes, Cell reports, 8, 1354, 10.1016/j.celrep.2014.07.030 · DOI
  5. 1954, Isolation of oligosaccharides enzymatically produced from hyaluronic acid, The Journal of biological chemistry, 208, 417, 10.1016/S0021-9258(18)65660-1 · DOI
  6. 1989, Solubilization and partial purification of hyaluronate synthetase from oligodendroglioma cells, The Journal of biological chemistry, 264, 11776, 10.1016/S0021-9258(18)80133-8 · DOI
  7. 10.1074/jbc.274.35.25085 · DOI · Paper page
  8. 10.1016/j.biochi.2009.10.006 · DOI
  9. 10.1136/ard.44.12.817 · DOI
  10. 10.1152/ajpgi.00494.2004 · DOI
  11. 10.1126/science.2408340 · DOI
  12. 10.1097/00006123-200206000-00023 · DOI
  13. 10.1523/JNEUROSCI.2695-17.2017 · DOI
  14. 10.1111/j.1471-4159.2012.07789.x · DOI
  15. 2009, High molecular weight hyaluronan decreases UVB-induced apoptosis and inflammation in human epithelial corneal cells, Mol Vis, 15, 577
  16. Takasugi M , et al. Naked mole-rat very-high-molecular-mass hyaluronan exhibits superior cytoprotective properties. Nature communications 11, 2376 (2020). · DOI
  17. Kulaberoglu Y , et al. The material properties of naked mole-rat hyaluronan. Sci Rep 9, 6632 (2019). · DOI
  18. Taguchi T , et al. Naked mole-rats are extremely resistant to post-traumatic osteoarthritis. Aging Cell 19, e13255 (2020). · DOI
  19. Zhao Y , Seluanov A , Gorbunova V . Revelations About Aging and Disease from Unconventional Vertebrate Model Organisms. Annu Rev Genet, (2021). · DOI
  20. Garantziotis S , Savani RC . Hyaluronan biology: A complex balancing act of structure, function, location and context. Matrix Biol 78-79, 1-10 (2019). · DOI
  21. Gupta RC , Lall R , Srivastava A , Sinha A . Hyaluronic Acid: Molecular Mechanisms and Therapeutic Trajectory. Front Vet Sci 6, 192 (2019). · DOI
  22. 10.4161/derm.21923 · DOI · Paper page
  23. 10.1073/pnas.1215432110 · DOI
  24. 10.1016/j.devcel.2016.12.017 · DOI
  25. 10.1074/jbc.M116.770149 · DOI
  26. 10.1016/j.matbio.2013.10.002 · DOI
  27. 10.1093/molbev/msm088 · DOI · Paper page
  28. 10.1186/s12915-021-01216-9 · DOI
  29. 10.1093/nar/gky427 · DOI
  30. 10.1093/nar/gkw1132 · DOI
  31. 10.1002/elps.200900140 · DOI
  32. Studer G , Tauriello G , Bienert S , Biasini M , Johner N , Schwede T . ProMod3-A versatile homology modelling toolbox. PLoS Comput Biol 17, e1008667 (2021). · DOI
  33. 10.1093/bioinformatics/btz828 · DOI
  34. 10.1093/bioinformatics/btu457 · DOI
  35. 10.1093/bioinformatics/btq662 · DOI
  36. Bertoni M , Kiefer F , Biasini M , Bordoli L , Schwede T . Modeling protein quaternary structure of homo-and hetero-oligomers beyond binary interactions by homology. Sci Rep 7, 10480 (2017). · DOI
  37. 10.1093/bioinformatics/btt473 · DOI · Paper page
  38. 10.1021/bi700382g · DOI
  39. 10.1073/pnas.071572898 · DOI
  40. 1999, Identification of bladder tumor-derived hyaluronidase: its similarity to HYAL1, Cancer research, 59, 4464
  41. 10.1038/ng.3198 · DOI
  42. Wang Y , Yang L . Genomic evidence for convergent molecular adaptation in electric fishes. Genome biology and evolution 13, evab038 (2021). · DOI
  43. 2020, Multiple genetic trajectories to extreme abiotic stress adaptation in Arctic Brassicaceae, Molecular biology and evolution, 37, 2052, 10.1093/molbev/msaa068 · DOI
  44. 10.1073/pnas.0701705104 · DOI
  45. Kimura M . The neutral theory of molecular evolution. Cambridge University Press (1983). · DOI
  46. Kosiol C , et al. Patterns of positive selection in six mammalian genomes. PLoS genetics 4, e1000144 (2008). · DOI · Paper page
  47. 10.1093/bioinformatics/bti042 · DOI · Paper page
  48. 10.1186/1471-2105-10-1 · DOI
  49. 10.4331/wjbc.v6.i3.110 · DOI
  50. 10.1016/B978-0-12-800092-2.00001-0 · DOI · Paper page
  51. 10.1073/pnas.96.11.6296 · DOI
  52. Faulkes CG , Davies KT , Rossiter SJ , Bennett NC . Molecular evolution of the hyaluronan synthase 2 gene in mammals: implications for adaptations to the subterranean niche and cancer resistance. Biol Lett 11, 20150185 (2015). · DOI
  53. 2020, Can gene-inactivating mutations lead to evolutionary novelty?, Current biology: CB, 30, R465, 10.1016/j.cub.2020.03.072 · DOI
  54. 10.1126/science.7209555 · DOI
  55. 10.1038/nature04578 · DOI
  56. Nevo E. Mosaic evolution of subterranean mammals: regression, progression, and global convergence. Oxford University Press (1999). · DOI
  57. 10.1126/science.aab3896 · DOI · Paper page
  58. 2019, Ventilatory, metabolic, and thermoregulatory responses of Damaraland mole rats to acute and chronic hypoxia, J Comp Physiol B, 189, 319, 10.1007/s00360-019-01206-y · DOI
  59. Campbell KL , et al. Molecular basis of a novel adaptation to hypoxic-hypercapnia in a strictly fossorial mole. BMC evolutionary biology 10, 214 (2010). · DOI
  60. 10.1074/jbc.M804178200 · DOI
  61. 10.2307/2406060 · DOI · Paper page
  62. 2021, Transposon-triggered innate immune response confers cancer resistance to the blind mole rat, Nat Immunol, 22, 1219, 10.1038/s41590-021-01027-8 · DOI · Paper page
  63. 1995, and Longevity in the Mole, Scalopus-Aquaticus (Mammalia, Insectivora), J Zool, 237, 107, 10.1111/j.1469-7998.1995.tb02750.x · DOI
  64. 10.1111/j.1474-9726.2006.00262.x · DOI
  65. 10.1111/j.1474-9726.2008.00431.x · DOI
  66. 2011, Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet journal, 17, 10, 10.14806/ej.17.1.200 · DOI · Paper page
  67. Pertea G , Pertea M. GFF utilities: GffRead and GffCompare. F1000Research 9, (2020). · DOI · Paper page
  68. Grabherr MG , et al. Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nature biotechnology 29, 644 (2011). · DOI
  69. 10.1186/1471-2105-10-1 · DOI
  70. Anders S , Huber W . Differential expression analysis for sequence count data. Nature Precedings, 1–1 (2010). · DOI
  71. 10.1186/gb-2014-15-1-r1 · DOI
  72. 10.1093/nar/gkv007 · DOI · Paper page
  73. 10.1186/s13059-022-02601-5 · DOI · Paper page
  74. 10.1089/omi.2011.0118 · DOI · Paper page
  75. 10.1016/j.matbio.2015.06.003 · DOI · Paper page
  76. 2020, A mutation map for human glycoside hydrolase genes, Glycobiology, 30, 500, 10.1093/glycob/cwaa010 · DOI
  77. 10.1038/s41580-020-00294-x · DOI
  78. 10.1093/nar/gkq443 · DOI
  79. 10.1073/pnas.0409137102 · DOI
  80. 2018, Limited evidence for parallel molecular adaptations associated with the subterranean niche in mammals: a comparative study of three superorders, Molecular biology and evolution, 35, 2544, 10.1093/molbev/msy161 · DOI
  81. 10.1093/molbev/msv175 · DOI
  82. Tsagkogeorga G , et al. A phylogenomic analysis of the role and timing of molecular adaptation in the aquatic transition of cetartiodactyl mammals. Royal Society open science 2, 150156 (2015). · DOI
  83. 10.1016/S0969-2126(00)00511-6 · DOI

Metadata

Authors
Zhao, Y., Zheng, Z., Zhang, Z., Hillpot, E., Lin, Y. S., Zakusilo, F. T., Lu, J. Y., Ablaeva, J., Miller, R. A., Nevo, E., Seluanov, A., & Gorbunova, V.
Affiliations
  • First Affiliated Hospital Zhejiang University (CN)
  • University of Rochester (US)
  • University of Michigan (US)
  • University of Haifa (IL)
  • University of Rochester Medicine (US)
Corresponding author
  • Seluanov, Andrei
  • Gorbunova, Vera
ORCID
Venue
Nature Communications
Publisher
openRxiv
Published
2023-05-09
Volume
14
Issue
1
Pages
8054-8054
ISSN
2041-1723 (ISSN-L)
DOI
10.1101/2023.05.08.539764
PMC
PMC10698142
OpenAlex
W4389333293
Cited by
34
References
1
Citations by year
2026: 12 · 2025: 9 · 2024: 12 · 2023: 1
FWCI
4.90
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Natural Science Foundation of China
  • National Institute on Aging (R01AG046320, R01AG027237, P01AG047200, R37AG046320, P01AG051449)
  • Natural Science Foundation of Zhejiang Province (LZ23C110002)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Subterranean biodiversity and taxonomy
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Tardigrade Biology and Ecology
Keywords
subterranean mammals, naked mole-rat, extracellular matrix, hyaluronan synthesis, hyaluronan degradation, gene expression regulation, hypoxia, oxidative stress, skin elasticity, tumor resistance, longevity, adaptive evolution

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