Structure and function of the transglutaminase cluster in the basal metazoan Halisarca dujardinii (sponge)

Мұқаба

Дәйексөз келтіру

Толық мәтін

Ашық рұқсат Ашық рұқсат
Рұқсат жабық Рұқсат берілді
Рұқсат жабық Тек жазылушылар үшін

Аннотация

Transglutaminases are enzymes that carry out post-translational modifications of proteins and participate in the regulation of their activities. Here, we show for the first time that the transglutaminase genes in the basal metazoan, sea sponge Halisarca dujardinii, are organized in a cluster, similar to mammalian transglutaminases. The regulatory regions of six transglutaminase genes and their differential expression in the course of H. dujardinii life cycle suggest independent regulation of these genes. The decrease in transglutaminase activities by cystamine facilitates restoration of the sponge multicellular structures after its mechanical dissociation. For the first time we observed that this decrease in transglutaminase activities was accompanied by generation of the reactive oxygen species in the cells of a basal metazoan. The study of transglutaminases in the basal metazoans and other sea-dwelling organisms might provide better understanding of evolution and specific functions of these enzymes in higher animals.

Толық мәтін

Рұқсат жабық

Авторлар туралы

A. Finoshin

Koltzov Institute of Developmental Biology, Russian Academy of Sciences

Хат алмасуға жауапты Автор.
Email: alexcolton@yandex.ru
Ресей, Moscow, 119334

O. Kravchuk

Koltzov Institute of Developmental Biology, Russian Academy of Sciences

Email: alexcolton@yandex.ru
Ресей, Moscow, 119334

K. Mikhailov

Lomonosov Moscow State University; Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences

Email: alexcolton@yandex.ru

Belozersky Institute of Physical and Chemical Biology

Ресей, Moscow, 119992; Moscow, 127051

R. Ziganshin

Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Email: alexcolton@yandex.ru
Ресей, Moscow, 117997

K. Adameyko

Koltzov Institute of Developmental Biology, Russian Academy of Sciences

Email: alexcolton@yandex.ru
Ресей, Moscow, 119334

V. Mikhailov

Koltzov Institute of Developmental Biology, Russian Academy of Sciences

Email: alexcolton@yandex.ru
Ресей, Moscow, 119334

Yu. Lyupina

Koltzov Institute of Developmental Biology, Russian Academy of Sciences

Email: alexcolton@yandex.ru
Ресей, Moscow, 119334

Әдебиет тізімі

  1. Shibata T., Kawabata S. (2018) Pluripotency and a secretion mechanism of Drosophila transglutaminase. J. Biochem. 163, 165–176.
  2. Lerner A., Matthias T. (2020) Processed food additive microbial transglutaminase and its cross-linked gliadin complexes are potential public health concerns in celiac disease. Int. J. Mol. Sci. 21, 1127.
  3. Della Mea M., Caparrós-Ruiz D., Claparols I., Serafini-Fracassini D., Rigau J. (2004) AtPng1p. The first plant transglutaminase. Plant Physiol. 135, 2046–2054.
  4. Eckert R.L., Kaartinen M.T., Nurminskaya M., Belkin A.M., Colak G., Johnson G.V., Mehta K. (2014) Transglutaminase regulation of cell function. Physiol. Rev. 94, 383–417.
  5. Nurminskaya M.V., Belkin A.M. (2012) Cellular functions of tissue transglutaminase. Int. Rev. Cell Mol. Biol. 294, 1–97.
  6. Ivashkin E., Melnikova V., Kurtova A., Brun N.R., Obukhova A., Khabarova M..Y, Yakusheff A., Adameyko I., Gribble K.E., Voronezhskaya E.E. (2019) Transglutaminase activity determines nuclear localization of serotonin immunoreactivity in the early embryos of invertebrates and vertebrates. ACS Chem. Neurosci. 10, 3888–3899.
  7. Zanetti L., Ristoratore F., Bertoni A., Cariello L. (2004) Characterization of sea urchin transglutaminase, a protein regulated by guanine/adenine nucleotides. J. Biol. Chem. 279, 49289–49297.
  8. Aaron L., Torsten M. (2019) Microbial transglutaminase: a new potential player in celiac disease. Clin. Immunol. 199, 37–43.
  9. Choi Y.-S., Jeong T.-J., Kim H.-W., Hwang K.-E., Sung J.-M., Seo D.-H., Kim Y.-B., Kim C.-J. (2017) Combined effects of sea mustard and transglutaminase on the quality characteristics of reduced-salt frankfurters: effect of transglutaminase and sea mustard on quality of sausages. J. Food Proc. Preservation. 41, e12945.
  10. Park Y.S., Choi Y.S., Hwang K.E., Kim T.K., Lee C.W., Shin D.M., Han S.G. (2017) Physicochemical properties of meat batter added with edible silkworm pupae (Bombyx mori) and transglutaminase. Korean J. Food Sci. Anim. Resourсе. 37, 351–359.
  11. Sun C.K., Ke C.J., Lin Y.W., Lin F.H., Tsai T.H., Sun J.S. (2021) Transglutaminase cross-linked gelatin-alginate-antibacterial hydrogel as the drug delivery-coatings for implant-related infections. Polymers. 13, 414.
  12. Porta R., Mariniello L., Di Pierro P., Sorrentino A., Giosafatto C.V. (2011) Transglutaminase crosslinked pectin- and chitosan-based edible films: a review. Crit. Rev. Food Sci. Nutr. 51, 223–238.
  13. Iismaa S.E., Mearns B.M., Lorand L., Graham R.M. (2009) Transglutaminases and disease: lessons from genetically engineered mouse models and inherited disorders. Physiol. Rev. 89, 991–1023.
  14. Lorand L., Graham R.M. (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4, 140–156.
  15. Baumgartner W., Golenhofen N., Weth A., Hiiragi T., Saint R., Griffin M., Drenckhahn D. (2004) Role of transglutaminase 1 in stabilisation of intercellular junctions of the vascular endothelium. Histochem. Cell Biol. 122, 17–25.
  16. Martinet N., Bonnard L., Regnault V., Picard E., Burke L., Siat J., Grosdidier G., Martinet Y., Vignaud J.M. (2003) In vivo transglutaminase type 1 expression in normal lung, preinvasive bronchial lesions, and lung cancer. Am. J. Respir. Cell. Mol. Biol. 28, 428–435.
  17. Fesus L., Piacentini M. (2002) Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem. Sci. 27, 534–539.
  18. Dubbink H.J., Cleutjens K.B., van der Korput H.A., Trapman J., Romijn J.C. (1999) An Sp1 binding site is essential for basal activity of the human prostate-specific transglutaminase gene (TGM4) promoter. Gene. 240, 261–267.
  19. Cassidy A.J., van Steensel M.A., Steijlen P.M., van Geel M., van der Velden J., Morley S.M., Terrinoni A., Melino G., Candi E., McLean W.H. (2005) A homozygous missense mutation in TGM5 abolishes epidermal transglutaminase 5 activity and causes acral peeling skin syndrome. Am. J. Hum. Genet. 77, 909–917.
  20. Board P.G., Webb G.C., McKee J., Ichinose A. (1988) Localization of the coagulation factor XIII A subunit gene (F13A) to chromosome bands 6p24–p25. Cytogenet. Cell Genet. 48, 25–27.
  21. Yang L., Shu H., Zhou M., Gong Y. (2022) Literature review on genotype–phenotype correlation in patients with hereditary spherocytosis. Clin. Genet. 102, 474–482.
  22. Wang R., Liang Z., Hal M., Söderhall K. (2001) A transglutaminase involved in the coagulation system of the freshwater crayfish, Pacifastacus leniusculus. Tissue localisation and cDNA cloning. Fish Shellfish Immunol. 11, 623–637.
  23. Cariello L., Ristoratore F., Zanetti L. (1997) A new transglutaminase‐like from the ascidian Ciona intestinalis. FEBS Lett. 408, 171–176.
  24. Mádi A., Punyiczki M., di Rao M., Piacentini M., Fésüs L. (1998) Biochemical characterization and localization of transglutaminase in wild‐type and cell‐death mutants of the nematode Caenorhabditis elegans. Eur. J. Biochem. 253, 583–590.
  25. Draper G.W., Shoemark D.K., Adams J.C. (2019) Modelling the early evolution of extracellular matrix from modern сtenophores and sponges. Essays Biochem. 63, 389–405.
  26. Li L., Watson C.J., Dubourd M., Bruton A., Xu M., Cooke G., Baugh J.A. (2016) HIF-1-dependent TGM1 expression is associated with maintenance of airway epithelial junction proteins. Lung. 194, 829–838.
  27. Liu T., Tee A.E., Porro A., Smith S.A., Dwarte T., Liu P.Y., Iraci N., Sekyere E., Haber M., Norris M.D., Diolaiti D., Della Valle G., Perini G., Marshall G.M. (2007) Activation of tissue transglutaminase transcription by histone deacetylase inhibition as a therapeutic approach for Myc oncogenesis. Proc. Natl. Acad. Sci. USA. 104, 18682–18687.
  28. Chhabra A., Verma A., Mehta K. (2009) Tissue transglutaminase promotes or suppresses tumors depending on cell context. Anticancer Res. 29(6), 1909–1919.
  29. Lee M.Y., Wu M.F., Cherng S.H., Chiu L.Y., Yang T.Y., Sheu G.T. (2018) Tissue transglutaminase 2 expression is epigenetically regulated in human lung cancer cells and prevents reactive oxygen species-induced apoptosis. Cancer Manag. Res. 10, 2835–2848.
  30. Su X., He X., Ben Q., Wang W., Song H., Ye Q., Zang Y., Li W., Chen P., Yao W., Yuan Y. (2017) Effect of p53 on pancreatic cancer-glucose tolerance abnormalities by regulating transglutaminase 2 in resistance to glucose metabolic stress. Oncotarget. 8, 74299–74311.
  31. Kim Y., Eom S., Kim K., Lee Y.S., Choe J., Hahn J.H., Lee H., Kim Y.M., Ha K.S., Ro J.Y., Jeoung D. (2010) Transglutaminase II interacts with rac1, regulates production of reactive oxygen species, expression of snail, secretion of Th2 cytokines and mediates in vitro and in vivo allergic inflammation. Mol. Immunol. 47, 1010–1022.
  32. Junkunlo K., Söderhäll K., Söderhäll I., Noonin C. (2016) Reactive oxygen species affect transglutaminase activity and regulate hematopoiesis in a Crustacean. J. Biol. Chem. 291, 17593–17601.
  33. Jeon J.H., Lee H.J., Jang G.Y., Kim C.W., Shim D.M., Cho S.Y., Yeo E.J., Park S.C., Kim I.G. (2004) Different inhibition characteristics of intracellular transglutaminase activity by cystamine and cysteamine. Exp. Mol. Med. 36, 576–581.
  34. Lee S.M., Jeong E.M., Jeong J., Shin D.M., Lee H.J., Kim H.J., Lim J., Lee J.H., Cho S.Y., Kim M.K., Wee W.R., Lee J.H., Kim I.G. (2012) Cysteamine prevents the development of lens opacity in a rat model of selenite-induced cataract. Invest. Ophthalmol. Vis. Sci. 53, 1452.
  35. Finoshin A.D., Adameyko K.I., Mikhailov K.V., Kravchuk O.I., Georgiev A.A., Gornostaev N.G., Kosevich I.A., Mikhailov V.S., Gazizova G.R., Shagimardanova E.I., Gusev O.A., Lyupina Y.V. (2020) Iron metabolic pathways in the processes of sponge plasticity. PLoS One. 15, e0228722.
  36. Adameyko K.I., Burakov A.V., Finoshin A.D., Mikhailov K.V., Kravchuk O.I., Kozlova O.S., Gornostaev N.G., Cherkasov A.V., Erokhov P.A., Indeykina M.I., Bugrova A.E., Kononikhin A.S., Moiseenko A.V., Sokolova O.S., Bonchuk A.N., Zhegalova I.V., Georgiev A.A., Mikhailov V.S., Gogoleva N.E., Gazizova G.R., Shagimardanova E.I., Gusev O.A., Lyupina Y.V. (2021) Conservative and atypical ferritins of sponges. Int. J. Mol. Sci. 22, 8635.
  37. Ereskovsky A. (2000) Reproduction cycles and strategies of the cold-water sponges Halisarca dujardini (Demospongiae, Halisarcida), Myxilla incrustans and Iophon piceus (Demospongiae, Poecilosclerida) from the White Sea. Biol. Bull. 198, 77–87.
  38. Кравчук О.И., Бураков А.В., Горностаев Н.Г., Михайлов К.В., Адамейко К.И., Финошин А.Д., Георгиев А.А., Михайлов В.С., Ерюкова Ю.Э., Рубиновский Г.А., Заиц Д.В., Газизова Г.Р., Гусев О.А., Шагимарданова Е.И., Люпина Ю.В. (2021) Деацетилазы гистонов в процессе реагрегации клеток губки Halisarca dujardinii. Онтогенез. 52, 367–383.
  39. Кравчук О.И., Финошин А.Д., Михайлов К.В., Зиганшин Р.Х., Адамейко К.И., Горностаев Н.Г., Жураковская А.И., Михайлов В.С., Шагимарданова Е.И., Люпина Ю.В. (2023) Характеристика дегидратазы δ-аминолевуленовой кислоты холодноводной губки Halisarca dujardinii. Молекуляр. биология. 57, 1085–1097.
  40. Haas B.J., Papanicolaou A., Yassour M., Grabherr M., Blood P.D., Bowden J., Couger M.B., Eccles D., Li B., Lieber M., MacManes M.D., Ott M., Orvis J., Pochet N., Strozzi F., Weeks N., Westerman R., William T., Dewey C.N., Henschel R., LeDuc R.D., Friedman N., Regev A. (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512.
  41. Altschul S. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25, 3389–3402.
  42. Zimin A.V., Marçais G., Puiu D., Roberts M., Salzberg S.L., Yorke J.A. (2013) The MaSuRCA genome assembler. Bioinformatics. 29, 2669–2677.
  43. Walker B.J., Abeel T., Shea T., Priest M., Abouelliel A., Sakthikumar S., Cuomo C.A., Zeng Q., Wortman J., Young S.K., Earl A.M. (2014) Pilon: аn integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 9, e112963.
  44. Robinson M.D., McCarthy D.J., Smyth G.K. (2010) еdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 26, 139–140.
  45. Emms D.M., Kelly S. (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238.
  46. Eddy S.R. (2011) Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195.
  47. Katoh K., Standley D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780.
  48. Capella-Gutierrez S., Silla-Martinez J.M., Gabaldon T. (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 25, 1972–1973.
  49. Nguyen L.T., Schmidt H.A., von Haeseler A., Minh B.Q. (2015) IQ-TREE: а fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274.
  50. Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods. 14, 587–589.
  51. Hoang D.T., Chernomor O., von Haeseler A., Minh B.Q., Vinh L.S. (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522.
  52. Kumar S., Stecher G., Tamura K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874.
  53. Wickham H. (2016) ggplot2: Elegant Graphics for Data Analysis. 2nd Ed. Switzerland: Springer, 260 p.
  54. Лапиков И.А., Могиленко Д.А., Диже Э.Б., Игнатович И.А., Орлов С.В., Перевозчиков А.П. (2008) Ap1-подобные цис-элементы в 5´-регуляторной области гена аполипопротеина A-I человека. Молекуляр. биология. 42, 295–305.
  55. Zhao W., Chow L.T., Broker T.R. (1999) A distal element in the HPV-11 upstream regulatory region contributes to promoter repression in basal keratinocytes in squamous epithelium. Virology. 253, 219–229.
  56. Wang G.L., Jiang B.H., Rue E.A., Semenza G.L. (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA. 92, 5510–5514.
  57. Dynan W.S., Tjian R. (1983) The promoter-specific transcription factor Sp1 binds to upstream sequences in the SV40 early promoter. Cell. 35, 79–87.
  58. Yee V.C., Pedersen L.C., Le Trong I., Bishop P.D., Stenkamp R.E., Teller D.C. (1994) Three-dimensional structure of a transglutaminase: human blood coagulation factor XIII. Proc. Natl. Acad. Sci. USA. 91, 7296–7300.
  59. Budillon A., Carbone C., Di Gennaro E. (2013) Tissue transglutaminase: a new target to reverse cancer drug resistance. Amino Acids. 44, 63–72.
  60. Min B., Chung K.C. (2018) New insight into transglutaminase 2 and link to neurodegenerative diseases. BMB Rep. 51, 5–13.
  61. Prat-Duran J., Pinilla E., Nørregaard R., Simonsen U., Buus N.H. (2021) Transglutaminase 2 as a novel target in chronic kidney disease – methods, mechanisms and pharmacological inhibition. Pharmacol. Ther. 222, 107787.
  62. He B.J., Liao L., Deng Z.F., Tao Y.F., Xu Y.C., Lin F.Q. (2018) Molecular genetic mechanisms of hereditary spherocytosis: current perspectives. Acta Haematol. 139, 60–66.
  63. Kamisawa T., Wood L.D., Itoi T., Takaori K. (2016) Pancreatic cancer. Lancet. 388, 73–85.
  64. Cho S.Y., Lee J.H., Ju M.K., Jeong E.M., Kim H.J., Lim J., Lee S., Cho N.H., Park H.H., Choi K., Jeon J.H., Kim I.G. (2015) Cystamine induces AIF-mediated apoptosis through glutathione depletion. Biochim. Biophys. Acta. 1853, 619–631.
  65. Akimov S.S., Belkin A.M. (2001) Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood. 98, 1567–1576.
  66. Li M., Wang X., Chen X., Hong J., Du Y., Song D. (2024) GK921, a transglutaminase inhibitor, strengthens the antitumor effect of cisplatin on pancreatic cancer cells by inhibiting epithelial-to-mesenchymal transition. Biochim. Biophys. Acta. 1870, 166925.
  67. Ferreira D., Naquet P., Manautou J. (2015) Influence of vanin-1 and catalytic products in liver during normal and oxidative stress conditions. Curr. Med. Chem. 22, 2407–2416.
  68. Jeitner T.M., Delikatny E.J., Ahlqvist J., Capper H., Cooper A.J. (2005) Mechanism for the inhibition of transglutaminase 2 by cystamine. Biochem. Pharmacol. 69, 961–970.
  69. Lorand L., Conrad S.M. (1984) Transglutaminases. Mol. Cell Biochem. 58, 9–35.
  70. Buznikov G.A., Nikitina L.A., Voronezhskaya E.E., Bezuglov V.V., Dennis Willows A.O., Nezlin L.P. (2003) Localization of serotonin and its possible role in early embryos of Tritonia diomedea (Mollusca: Nudibranchia). Cell Tissue Res. 311, 259–266.
  71. Glebov K., Voronezhskaya E.E., Khabarova M.Y., Ivashkin E., Nezlin L.P., Ponimaskin E.G. (2014) Mechanisms underlying dual effects of serotonin during development of Helisoma trivolvis (Mollusca). BMC Dev. Biol. 14, 14.
  72. Vacelet J., Donadey C. (1977) Electron microscope study of the association between some sponges and bacteria. J. Exp. Mar. Biol. Ecol. 30, 301–314.
  73. Calcabrini C., Catanzaro E., Bishayee A., Turrini E., Fimognari C. (2017) Marine sponge natural products with anticancer potential: an updated review. Mar. Drugs. 15, 310.

Қосымша файлдар

Қосымша файлдар
Әрекет
1. JATS XML
2. Fig. 1. Phylogenetic tree of animal TGM. Numbers on tree nodes correspond to node support estimates using the ultrafast bootstrap method UFBoot with 1000 replicates.

Жүктеу (1MB)
3. Fig. 2. TGM genes of the sponge H. dujardinii (a) and humans (б). The numbers indicate the distances between genes in nucleotide pairs. The 5´ region of the H. dujardinii sponge genes shows regulatory sequences: TATA box; HRE – hypoxia response element; AP1, SP1, CREB/AP1 – binding sites with the corresponding transcription factors.

Жүктеу (238KB)
4. Fig. 3. Expression of TGM genes during dissociation/reaggregation of the sponge H. dujardinii in different periods of the annual cycle. The left panel shows the gene expression level in the sponge body tissue in different periods of the annual cycle. Blue, light green, pink, and orange colors indicate winter, spring, summer, and autumn, respectively. *Statistically significant differences in TGM gene expression in the sponge body tissue in different seasons. The right panel shows the change in expression in dissociated cells and cell aggregates compared to the intact sponge. Large and small dots indicate dissociated cells and aggregates. Only statistically significant differences (FDR < 0.001, see Experimental Section) are shown on the heat map on the right.

Жүктеу (227KB)
5. Fig. 4. Alignment of the amino acid sequences of the catalytic sites of H. dujardinii and human TGM. Arrows and boxes highlight the catalytic residues cysteine ​​376 (Cys376), histidine 435 (His435), and aspartic acid 458 (Asp458), which are essential for catalytic activity. Substitutions of key amino acids are shown in blue. The numbering is given for H. sapiens TGM1.

Жүктеу (493KB)
6. Fig. 5. Electrophoretic analysis of proteins in 10% SDS-PAGE, stained with Coomassie R250. M – molecular weight marker; H. d. – clarified homogenate of H. dujardinii cell suspension. The arrow indicates the zone used for identification of H. dujardinii TGM by mass spectrometry.

Жүктеу (80KB)
7. Fig. 6. Cell suspension 2 h after sponge dissociation. a – Control. б–г – Suspension in the presence of 1, 5, 25 mM cystamine. Scale bar – 50 µm.

Жүктеу (572KB)
8. Fig. 7. Cell aggregates 24 h after sponge dissociation, formed in the absence (a) and presence of cystamine at a concentration of 1 mM (б); 5 mM (в) and 25 mM (г). Scale bar – 100 µm. д – Comparative analysis of aggregate area.

Жүктеу (181KB)
9. Fig. 8. Confocal microscopy of a suspension of H. dujardinii sponge cells. Green color shows the fluorescence of cells after adding H2DCFDA to the incubation medium. White arrows show small round cells, black arrows show large cells with outgrowths.

Жүктеу (130KB)
10. Fig. 9. Fluorescence of cell aggregates after adding H2DCFDA to the incubation medium. а,б – Control. In the presence of cystamine: в,г – 1 mM; д,е – 5 mM; g, h – 25 mM. и – Comparative analysis of fluorescence intensity.

Жүктеу (230KB)

© Russian Academy of Sciences, 2024