Wikipedia

Tardigrade specific proteins

Tardigrade specific proteins are types of intrinsically disordered proteins specific to tardigrades. These proteins help tardigrades survive desiccation, one of the adaptations which contribute to tardigrade's extremotolerant nature. Tardigrade specific proteins are strongly influenced by their environment, leading to adaptive malleability across a variety of extreme abiotic environments.

History

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The mechanisms of tardigrade desiccation protection were originally thought to result from high levels of the sugar trehalose. Trehalose is used by organisms like yeast to avoid desiccation in dry environments by working with heat shock proteins[1] to keep desiccation-sensitive proteins in solution.[2][3] However, while tardigrades can accumulate small levels of trehalose, the levels are insufficient to provide protection from extreme conditions.[4] Other molecules which help certain organisms avoid cellular desiccation include late embryogenesis abundant proteins, which provide protection to embryonic cotton seeds.[5] Certain proteins actually responsible for the tardigrade's hardiness, including the cytoplasmic and secreted abundant heat soluble proteins, were discovered when searching for late embryogenesis abundant proteins in tardigrades.[6]

One strategy used by the tardigrade to survive in dry environments is anhydrobiosis. Anhydrobiosis is a process in which an organism can lose nearly all of its water and enter an ametabolic state.[7]

Function

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Tardigrade specific proteins are a type of intrinsically disordered proteins, which have no predetermined shape or task. These proteins use many different conformations, called an ensemble, to move through different structures. Because of this, intrinsically disordered proteins may react strongly to the environment they inhabit.[8] There are three families of tardigrade specific proteins, each named after where the protein is localized within a cell. These proteins are similar to late embryogenesis abundant proteins but are specific to tardigrades. The three families do not resemble each other and are expressed or enriched during desiccation. Unlike traditional proteins, intrinsically disordered proteins do not precipitate out of solution or denature during high heat.[9] Tardigrades rely on these proteins to help them survive extreme environments, where they put their bodies in a dehydrated state called a tun. In most organisms, dehydration causes problems for cells, which need a hydrated environment for their proteins to function. However, tardigrade specific proteins assist in preventing aggregation of cell contents upon dehydration, and maintain the integrity of the cell membrane upon rehydration.

Types

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Cytoplasmic

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Cytoplasmic abundant heat soluble (CAHS) proteins are highly expressed in response to desiccation. There are two hypotheses for their function in tardigrades. The vitrification hypothesis is the idea that, when a tardigrade becomes desiccated, the viscosity within its cells increases to the point that denaturation and membrane fusion in proteins would stop.[10] A second hypothesis, the water replacement hypothesis, posits that CAHS proteins replace water in other desiccation-sensitive proteins, protecting the hydrogen bonds normally reliant on water.[11] CAHS proteins are dispersed throughout the cell in normal conditions, but form a network of filaments during environmentally stressful conditions. This network transforms the cytoplasm into a gel-like matrix and prevents the cell from collapsing as water leaches out.[12] This state is reversible and the proteins disaggregate when exposed to less stressful conditions.[13]

When forming the filament network, CAHS proteins have long helical domains that interact in a coiled manner with each other. These interactions are possible due to the proteins' partial disorder, with two flexible tails surrounding the helical domains.[14]

CAHS proteins have been studied to observe their interactions with trehalose, a sugar used by other species to prevent desiccation. Trehalose was found to interact at higher levels with CAHS proteins than other sugars such as sucrose.[15] Trehalose averages only 1% in most species of tardigrades, and in no species more than 3%, indicating that tardigrades use other strategies to tolerate dehydration.[6]

Tardigrade CAHS protein injected into mice produced no inflammatory response or hemolysis.[16]

Secreted

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Secreted abundant heat soluble (SAHS) proteins are similar to fatty acid-binding proteins, notably in their structure with an antiparallel beta-barrel and internal fatty acid binding pocket.[17][18] SAHS proteins are often secreted into media and associated with special extracellular structures.[19] Dried tardigrades have an abundance of secretory cells which are not found in hydrated individuals. The mechanism behind SAHS proteins has not yet been determined, but the presence of secretory cells only during desiccation suggests they are used to protect cells during periods of dehydration.

Mitochondrial

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Mitochondrial abundant heat soluble (MAHS) proteins are localized in mitochondria and are responsible for protecting mitochondria during desiccation.[20] Because of its role in metabolizing reactive oxygen species, the mitochondrion is an important organelle to protect in extreme environments. During dehydration, the mitochondria of tardigrades grow much smaller and lose their cristae.[5] MAHS proteins may act to replace water in the membrane of the mitochondria, preventing uneven rehydration and membrane rupture.[21] Mitochondria and muscle contraction due to mitochondria are essential for tardigrade to enter the "tun" state of anhydrobiosis.[22]

Dsup (damage suppressor protein)

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Dsup is a DNA-associating protein, unique to the tardigrade,[23] that suppresses the occurrence of DNA breaks by radiation.[24][25][26][27] Dsup localized to nuclear DNA reduces single-strand breaks and double-strand breaks when subjected to ionizing radiation.[28]

LEA Proteins

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Late embryogenesis abundant proteins (LEA proteins) are proteins that protect against protein aggregation due to dehydration or osmotic stress. However, no LEA proteins have been found in tardigrades.[6]

References

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  1. ^ Kim SX, Çamdere G, Hu X, Koshland D, Tapia H (July 2018). Storz G, Hyman AA (eds.). "Synergy between the small intrinsically disordered protein Hsp12 and trehalose sustain viability after severe desiccation". eLife. 7: e38337. doi:10.7554/eLife.38337. PMC 6054528. PMID 30010539.
  2. ^ Tapia H, Young L, Fox D, Bertozzi CR, Koshland D (May 2015). "Increasing intracellular trehalose is sufficient to confer desiccation tolerance to Saccharomyces cerevisiae". Proceedings of the National Academy of Sciences of the United States of America. 112 (19): 6122–6127. Bibcode:2015PNAS..112.6122T. doi:10.1073/pnas.1506415112. PMC 4434740. PMID 25918381.
  3. ^ Bellavia G, Giuffrida S, Cottone G, Cupane A, Cordone L (May 2011). "Protein thermal denaturation and matrix glass transition in different protein-trehalose-water systems". The Journal of Physical Chemistry B. 115 (19): 6340–6346. doi:10.1021/jp201378y. PMID 21488647.
  4. ^ Boothby TC, Tapia H, Brozena AH, Piszkiewicz S, Smith AE, Giovannini I, et al. (March 2017). "Tardigrades Use Intrinsically Disordered Proteins to Survive Desiccation". Molecular Cell. 65 (6): 975–984.e5. doi:10.1016/j.molcel.2017.02.018. PMC 5987194. PMID 28306513.
  5. ^ a b Hesgrove C, Boothby TC (November 2020). "The biology of tardigrade disordered proteins in extreme stress tolerance". Cell Communication and Signaling. 18 (1): 178. doi:10.1186/s12964-020-00670-2. PMC 7640644. PMID 33148259.
  6. ^ a b c Yamaguchi A, Tanaka S, Kunieda T (2012). "Two novel heat-soluble protein families abundantly expressed in an anhydrobiotic tardigrade". PLOS One. 7 (8): e44209. Bibcode:2012PLoSO...744209Y. doi:10.1371/journal.pone.0044209. PMC 3429414. PMID 22937162.
  7. ^ Giovannini I, Boothby TC, Cesari M, Goldstein B, Guidetti R, Rebecchi L (February 2022). "Production of reactive oxygen species and involvement of bioprotectants during anhydrobiosis in the tardigrade Paramacrobiotus spatialis". Scientific Reports. 12 (1): 1938. Bibcode:2022NatSR..12.1938G. doi:10.1038/s41598-022-05734-6. PMC 8816950. PMID 35121798.
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  9. ^ Uversky VN (October 2003). "A protein-chameleon: conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders". Journal of Biomolecular Structure & Dynamics. 21 (2): 211–234. doi:10.1080/07391102.2003.10506918. PMID 12956606. S2CID 824815.
  10. ^ Sakurai M, Furuki T, Akao K, Tanaka D, Nakahara Y, Kikawada T, et al. (April 2008). "Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki". Proceedings of the National Academy of Sciences of the United States of America. 105 (13): 5093–5098. Bibcode:2008PNAS..105.5093S. doi:10.1073/pnas.0706197105. PMC 2278217. PMID 18362351.
  11. ^ Crowe LM (March 2002). "Lessons from nature: the role of sugars in anhydrobiosis". Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology. 131 (3): 505–513. doi:10.1016/S1095-6433(01)00503-7. PMID 11867276.
  12. ^ Tanaka A, Nakano T, Watanabe K, Masuda K, Honda G, Kamata S, et al. (September 2022). "Stress-dependent cell stiffening by tardigrade tolerance proteins that reversibly form a filamentous network and gel". PLOS Biology. 20 (9). Live Science: e3001780. doi:10.1371/journal.pbio.3001780. PMC 9592077. PMID 36067153.
  13. ^ Tanaka A, Nakano T, Watanabe K, Masuda K, Honda G, Kamata S, et al. (September 2022). "Stress-dependent cell stiffening by tardigrade tolerance proteins that reversibly form a filamentous network and gel". PLOS Biology. 20 (9): e3001780. doi:10.1371/journal.pbio.3001780. PMC 9592077. PMID 36067153.
  14. ^ Malki A, Teulon JM, Camacho-Zarco AR, Chen SW, Adamski W, Maurin D, et al. (January 2022). "Intrinsically Disordered Tardigrade Proteins Self-Assemble into Fibrous Gels in Response to Environmental Stress". Angewandte Chemie. 61 (1): e202109961. doi:10.1002/anie.202109961. PMC 9299615. PMID 34750927.
  15. ^ Nguyen K, Kc S, Gonzalez T, Tapia H, Boothby TC (October 2022). "Trehalose and tardigrade CAHS proteins work synergistically to promote desiccation tolerance". Communications Biology. 5 (1): 1046. doi:10.1038/s42003-022-04015-2. PMC 9526748. PMID 36182981.
  16. ^ Esterly HJ, Crilly CJ, Christian BE (2020). "Toxicity and Immunogenicity of a Tardigrade Cytosolic Abundant Heat Soluble Protein in Mice". Frontiers in Pharmacology. 11: 565969. doi:10.3389/fphar.2020.565969. PMC 7577191. PMID 33117164.
  17. ^ Fukuda Y, Miura Y, Mizohata E, Inoue T (August 2017). "Structural insights into a secretory abundant heat-soluble protein from an anhydrobiotic tardigrade, Ramazzottius varieornatus". FEBS Letters. 591 (16): 2458–2469. doi:10.1002/1873-3468.12752. PMID 28703282. S2CID 3434502.
  18. ^ Fukuda Y, Inoue T (May 2018). "Crystal structure of secretory abundant heat soluble protein 4 from one of the toughest "water bears" micro-animals Ramazzottius Varieornatus". Protein Science. 27 (5): 993–999. doi:10.1002/pro.3393. PMC 5916119. PMID 29493034.
  19. ^ Richaud M, Le Goff E, Cazevielle C, Ono F, Mori Y, Saini NL, et al. (March 2020). "Ultrastructural analysis of the dehydrated tardigrade Hypsibius exemplaris unveils an anhydrobiotic-specific architecture". Scientific Reports. 10 (1): 4324. Bibcode:2020NatSR..10.4324R. doi:10.1038/s41598-020-61165-1. PMC 7062702. PMID 32152342.
  20. ^ Tanaka S, Tanaka J, Miwa Y, Horikawa DD, Katayama T, Arakawa K, et al. (2015-02-12). "Novel mitochondria-targeted heat-soluble proteins identified in the anhydrobiotic Tardigrade improve osmotic tolerance of human cells". PLOS ONE. 10 (2): e0118272. Bibcode:2015PLoSO..1018272T. doi:10.1371/journal.pone.0118272. PMC 4326354. PMID 25675104.
  21. ^ Popova AV, Hundertmark M, Seckler R, Hincha DK (July 2011). "Structural transitions in the intrinsically disordered plant dehydration stress protein LEA7 upon drying are modulated by the presence of membranes". Biochimica et Biophysica Acta (BBA) - Biomembranes. 1808 (7): 1879–1887. doi:10.1016/j.bbamem.2011.03.009. PMID 21443857.
  22. ^ Halberg KA, Jørgensen A, Møbjerg N (2013). "Desiccation tolerance in the tardigrade Richtersius coronifer relies on muscle mediated structural reorganization". PLOS One. 8 (12): e85091. Bibcode:2013PLoSO...885091H. doi:10.1371/journal.pone.0085091. PMC 3877342. PMID 24391987.
  23. ^ Zimmer, Carl (12 April 2024). "What Makes Tiny Tardigrades Nearly Radiation Proof - New research finds that the microscopic "water bears" are remarkably good at repairing their DNA after a huge blast of radiation". The New York Times. Archived from the original on 12 April 2024. Retrieved 13 April 2024.
  24. ^ Hashimoto T, Kunieda T (June 2017). "DNA Protection Protein, a Novel Mechanism of Radiation Tolerance: Lessons from Tardigrades". Life. 7 (2): 26. Bibcode:2017Life....7...26H. doi:10.3390/life7020026. PMC 5492148. PMID 28617314.
  25. ^ Turk V (20 September 2016). "Scientists Identify Gene That Protects Tardigrades From Radiation". Vice. Retrieved 19 May 2018.
  26. ^ Tauger N, Gill V (20 September 2016). "Survival secret of 'Earth's hardiest animal' revealed". BBC News. Retrieved 2016-09-21.
  27. ^ Hashimoto T, Horikawa DD, Saito Y, Kuwahara H, Kozuka-Hata H, Shin-I T, Minakuchi Y, Ohishi K, Motoyama A, Aizu T, Enomoto A, Kondo K, Tanaka S, Hara Y, Koshikawa S, Sagara H, Miura T, Yokobori SI, Miyagawa K, Suzuki Y, Kubo T, Oyama M, Kohara Y, Fujiyama A, Arakawa K, Katayama T, Toyoda A, Kunieda T (September 2016). "Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein". Nature Communications. 7: 12808. Bibcode:2016NatCo...712808H. doi:10.1038/ncomms12808. PMC 5034306. PMID 27649274.
  28. ^ Aguilar R, Hickman AR, Tyler JK (2023). "Multivalent binding of the tardigrade Dsup protein to chromatin promotes yeast survival and longevity upon exposure to oxidative damage". Research Square: rs.3.rs–3182883. doi:10.21203/rs.3.rs-3182883/v1. PMC 10402244. PMID 37546815.
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