93
Views
0
CrossRef citations to date
0
Altmetric
Research article

HIF-1α interacting with miR-2013-3p regulates pathogen-induced energy production changes via targeting glutamate dehydrogenase in the sea urchin Strongylocentrotus intermedius

, , , , ORCID Icon &
Article: 2367660 | Received 20 Dec 2023, Accepted 09 Jun 2024, Published online: 18 Jun 2024

References

  • Cai X, Zhou Z, Zhu J, et al. Zebrafish HIF-3α modulates erythropoiesis via regulation of gata1 to facilitate hypoxia tolerance. Development. 2020;147(22):dev185116. doi: 10.1242/dev.185116
  • Choudhry H, Harris AL. Advances in hypoxia-inducible factor biology. Cell Metab. 2018;27(2):281–17. doi: 10.1016/j.cmet.2017.10.005
  • Law SH, Wu RS, Ng PK, et al. Cloning and expression analysis of two distinct HIF-alpha isoforms – gcHIF-1alpha and gcHIF-4alpha – from the hypoxia-tolerant grass carp, Ctenopharyngodon idellus. BMC Mol Biol. 2006;7(1):15. doi: 10.1186/1471-2199-7-15
  • Rissanen E, Tranberg HK, Sollid J, et al. Temperature regulates hypoxia-inducible factor-1 (HIF-1) in a poikilothermic vertebrate, crucian carp (Carassius carassius). J Exp Biol. 2006;209(Pt6):994–1003. doi: 10.1242/jeb.02103
  • Poyya J, Joshi CG, Kumar DJ, et al. Sequence analysis and phylogenetic studies of hypoxia-inducible factor-1α. Cancer Inform. 2017;16:1176935117712242. doi: 10.1177/1176935117712242
  • He J, Yu Y, Qin XW, et al. Identification and functional analysis of the Mandarin fish (Siniperca chuatsi) hypoxia-inducible factor-1α involved in the immune response. Fish Shellfish Immunol. 2019;92:141–150. doi: 10.1016/j.fsi.2019.04.298
  • Lin Y, Miao LH, Liu B, et al. Molecular cloning and functional characterization of the hypoxia-inducible factor-1α in bighead carp (Aristichthys nobilis). Fish Physiol Biochem. 2021;47(2):351–364. doi: 10.1007/s10695-020-00917-2
  • Ramberg S, Høyheim B, Østbye TK, et al. A de novo full-length mRNA transcriptome generated from hybrid-corrected pacbio long-reads improves the transcript annotation and identifies thousands of novel splice variants in Atlantic Salmon. Front Genet. 2021;12:656334. doi: 10.3389/fgene.2021.656334
  • Li T, Brouwer M. Hypoxia-inducible factor, gsHIF, of the grass shrimp Palaemonetes pugio: molecular characterization and response to hypoxia. Comp Biochem Phys B. 2007;147(1):11–19. doi: 10.1016/j.cbpb.2006.12.018
  • Soñanez-Organis JG, Peregrino-Uriarte AB, Gómez-Jiménez S, et al. Molecular characterization of hypoxia inducible factor-1 (HIF-1) from the white shrimp Litopenaeus vannamei and tissue-specific expression under hypoxia. Comp Biochem Phys C. 2009;150(3):395–405. doi: 10.1016/j.cbpc.2009.06.005
  • Piontkivska H, Chung JS, Ivanina AV, et al. Molecular characterization and mRNA expression of two key enzymes of hypoxia-sensing pathways in eastern oysters Crassostrea virginica (Gmelin): hypoxia-inducible factor α (HIF-α) and HIF-prolyl hydroxylase (PHD). Comp Biochem Phys D. 2011;6(2):103–114. doi: 10.1016/j.cbd.2010.10.003
  • Kawabe S, Yokoyama Y. Role of hypoxia-inducible factor α in response to hypoxia and heat shock in the Pacific oyster Crassostrea gigas. Mar Biotechnol (NY). 2012;14(1):106–119. doi: 10.1007/s10126-011-9394-3
  • Cai X, Huang Y, Zhang X, et al. Cloning, characterization, hypoxia and heat shock response of hypoxia inducible factor-1 (HIF-1) from the small abalone Haliotis diversicolor. Gene. 2014;534(2):256–264. doi: 10.1016/j.gene.2013.10.048
  • Wang S, Zhang J, Jiao W, et al. Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat Ecol Evol. 2017;1(5):120. doi: 10.1038/s41559-017-0120
  • Rimoldi S, Terova G, Ceccuzzi P, et al. HIF-1α mRNA levels in Eurasian perch (perca fluviatilis) exposed to acute and chronic hypoxia. Mol Biol Rep. 2012;39(4):4009–4015. doi: 10.1007/s11033-011-1181-8
  • Mohindra V, Tripathi RK, Singh RK, Lal KK. Molecular characterization and expression analysis of three hypoxia-inducible factor alpha subunits, HIF-1α, -2α and -3α in hypoxia-tolerant Indian catfish, Clarias batrachus [Linnaeus, 1758]. Mol Biol Rep. 2013;40(10):5805–5815. doi: 10.1007/s11033-013-2685-1
  • Zhang G, Zhao C, Wang Q, et al. Identification of HIF-1 signaling pathway in pelteobagrus vachelli using RNA-Seq: effects of acute hypoxia and reoxygenation on oxygen sensors, respiratory metabolism, and hematology indices. J Comp Physiol B. 2017;187(7):931–943. doi: 10.1007/s00360-017-1083-8
  • Sun JL, Zhao LL, Wu H, et al. Acute hypoxia changes the mode of glucose and lipid utilization in the liver of the largemouth bass (Micropterus salmoides). Sci Total Environ. 2020;713:135157. doi: 10.1016/j.scitotenv.2019.135157
  • Lee P, Chandel NS, Simon MC. Cellular adaptation to hypoxia through hypoxia inducible factors and beyond. Nat Rev Mol Cell Biol. 2020;21(5):268–283. doi: 10.1038/s41580-020-0227-y
  • Hochachka P, Buck L, Doll C, et al. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci U S A. 1996;93(18):9493–9498. doi: 10.1073/pnas.93.18.9493
  • Lutz PL, Nilsson GE, Prentice HM. The brain without oxygen: causes of failure-physiological and molecular mechanisms for survival. Kluwer Academic; 1994. doi: 10.16958/drsr.2014.12.3.227
  • Nilsson GE, Ostlund-Nilsson S. Does size matter for hypoxia tolerance in fish. Biol Rev Camb Philos Soc. 2008;83(2):173–189. doi: 10.1111/j.1469-185X.2008.00038.x
  • Yang S, Yan T, Wu H, et al. Acute hypoxic stress: effect on blood parameters, antioxidant enzymes, and expression of HIF-1alpha and GLUT-1 genes in largemouth bass (Micropterus salmoides). Fish Shellfish Immunol. 2017;67:449–458. doi: 10.1016/j.fsi.2017.06.035
  • Chen X, Liu Z, Gu Y, et al. A hexokinase from the oyster Crassostrea gigas is involved in immune recognition as a pattern recognition receptor. Dev Comp Immunol. 2021;122:104083. doi: 10.1016/j.dci.2021.104083
  • Brahimi-Horn MC, Pouysségur J. HIF at a glance. J Cell Sci. 2009;122(Pt8):1055–1057. doi: 10.1242/jcs.035022
  • So JH, Kim JD, Yoo KW, et al. FIH-1, a novel interactor of mindbomb, functions as an essential anti-angiogenic factor during zebrafish vascular development. PLoS One. 2014;9(10):e109517. doi: 10.1371/journal.pone.0109517
  • Bracken CP, Whitelaw ML, Peet DJ. The hypoxia-inducible factors: key transcriptional regulators of hypoxic responses. Cell Mol Life Sci. 2003;60(7):1376–1393. doi: 10.1007/s00018-003-2370-y
  • Lawrence JM. Sea urchin life-history strategies. Sea Urchins: biol And Ecol. 2020;43:19–28. doi: 10.1016/b978-0-12-819570-3.00002-0
  • Smith LC, Clow LA, Terwilliger DP. The ancestral complement system in sea urchins. Immunol Rev. 2001;180(1):16–34. doi: 10.1034/j.1600-065x.2001.1800102.x
  • Smith LC. Diversification of innate immune genes: lessons from the purple sea urchin. Dis Model Mech. 2010;3(5–6):274–279. doi: 10.1242/dmm.004697
  • Buchmann K. Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol. 2014;5:459. doi: 10.3389/fimmu.2014.00459
  • Zhang Q, Cao X. Epigenetic remodeling in innate immunity and inflammation. Annu Rev Immunol. 2021;39(1):279–311. doi: 10.1146/annurev-immunol-093019-123619
  • Auguste M, Melillo D, Corteggio A, et al. Methodological approaches to assess innate immunity and innate memory in marine invertebrates and humans. Front Toxicol. 2022;4:842469. doi: 10.3389/ftox.2022.842469
  • Miranda-Cruz MM, Poom-Llamas JJ, Godoy-Lugo JA, et al. Silencing of HIF-1 in WSSV-infected white shrimp: effect on viral load and antioxidant enzymes. Comp Biochem Phys C. 2018;213:19–26. doi: 10.1016/j.cbpc.2018.07.004
  • Cao Y, Fang T, Du Y, et al. MiR-2013 negatively regulates phylogenetically conserved PIP5K involved in TLR4 mediated immune responses of amphioxus (Branchiostoma belcheri Tsingtaunese). Dev Comp Immunol. 2022;133:104430. doi: 10.1016/j.dci.2022.104430
  • Thomas JR, Lee A. Measuring Ca2+-dependent modulation of voltage-gated Ca2+ channels in HEK-293T cells. Cold Spring Harb Protoc. 2016;2016(9):db.prot087213. doi: 10.1101/pdb.prot087213
  • Mügge FLB, Morlock GE. Planar bioluminescent cytotoxicity assay via genetically modified adherent human reporter cell lines, applied to authenticity screening of Saussurea costus root. J Chromatogr A. 2022;1683:463522. doi: 10.1016/j.chroma.2022.463522
  • Liu Z, Ma F, Kang Y, et al. Gene ssa-MiR-301a-3p improves rainbow trout (Oncorhynchus mykiss) resistance to heat stress by targeting hsp90b2. PeerJ. 2022;10:e13476. doi: 10.7717/peerj.13476
  • He L, Zhao M, Yu X, et al. MicroRNA-182-3p negatively regulates cytokines expression by targeting TLR5M in orange-spotted grouper, Epinephelus coioides. Fish Shellfish Immunol. 2019;93:589–596. doi: 10.1016/j.fsi.2019.07.063
  • Ren L, Li L, Zhan Y, et al. Isolation of a new PAK1 gene from sea cucumber (Apostichopus japonicus) and its expression analysis and function characterization. J Ocean Univ China. 2019;18(5):1147–1157. doi: 10.1007/s11802-019-4034-z
  • Liu L, Zhao T, Lin K, et al. Identification of a novel RhoA gene in the sea cucumber Apostichopus japonicus and its immune regulatory function via interacting with MiR-2012-5p. Int j biol macromol. 2022;203:572–582. doi: 10.1016/j.ijbiomac.2022.01.176
  • Ryu TK, Lee G, Rhee Y, et al. Identification of nickel response genes in abnormal early developments of sea urchin by differential display polymerase chain reaction. Ecotoxicol Environ Saf. 2012;84:18–24. doi: 10.1016/j.ecoenv.2012.06.018
  • Cui D, Liu L, Zhao T, et al. Responses of sea urchins (Strongylocentrotus intermedius) with different sexes to CO2-induced seawater acidification: histology, physiology, and metabolomics. Mar Pollut Bull. 2022;178:113606. doi: 10.1016/j.marpolbul.2022.113606
  • Guo C, Zhang Z, Zhang M, et al. Screening and stability analysis of reference genes for gene expression normalization in hybrid yellow catfish (Pelteobagrus fulvidraco ♀ × Pelteobagrus vachelli ♂) fed diets containing different soybean meal levels. Aquac Nutr. 2023;2023:1–17. doi: 10.1155/2023/1232518
  • Jiao R, Wu B, Han S, et al. miRn-3 inhibits cutaneous wound healing by targeting gelsolin in the sea cucumber Apostichopus japonicus. Int J Biol Macromol. 2024;254(Pt 2):127801. doi: 10.1016/j.ijbiomac.2023.127801
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔct method. Methods. 2001;25(4):402–408. doi: 10.1006/meth.2001.1262
  • Zhao T, Ren L, Li C, et al. MiR-7 regulates pathogen-induced immune response via PAK1 in the sea cucumber Apostichopus japonicus. Front Immunol. 2022;13:927796. doi: 10.3389/fimmu.2022.927796
  • Li C, Zhao T, Ren L, et al. Characterization of a novel glutamate dehydrogenase gene and its response to heat stress in the sea urchin Strongylocentrotus intermedius. Aquacult Rep. 2023;28:101446. doi: 10.1016/j.aqrep.2022.101446
  • Zhao T, Liu L, Li C, et al. Isolation and characterization of four pathogenic strains of Vibrio spp. From farmed sea urchins. Strongylocentrotus Intermedius, China Microb Pathog. 2022;169:105651. doi: 10.1016/j.micpath.2022.105651
  • Wang T, Meng J, Li L, et al. Characterization of CgHIFα-Like, a novel bHLH-PAS transcription factor family member, and its role under hypoxia stress in the pacific oyster Crassostrea gigas. PLoS One. 2016;11(11):e0166057. doi: 10.1371/journal.pone.0166057
  • Jiang H, Guo R, Powell-Coffman JA. The Caenorhabditis elegans hif-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia. Proc Natl Acad Sci U S A. 2001;98(14):7916–7921. doi: 10.1073/pnas.141234698
  • Okamura Y, Mekata T, Elshopakey GE, et al. Molecular characterization and gene expression analysis of hypoxia-inducible factor and its inhibitory factors in kuruma shrimp Marsupenaeus japonicus. Fish Shellfish Immunol. 2018;79:168–174. doi: 10.1016/j.fsi.2018.05.015
  • Guan F, Lu XJ, Li CH, et al. Molecular characterization of mudskipper (Boleophthalmus pectinirostris) hypoxia-inducible factor-1α (HIF-1α) and analysis of its function in monocytes/macrophages. PLoS One. 2017;12(5):e0177960. doi: 10.1371/journal.pone.0177960
  • Wang C, Wu X, Hu X, et al. Hypoxia-inducible factor 1α from a high-altitude fish enhances cytoprotection and elevates nitric oxide production in hypoxic environment. Fish Physiol Biochem. 2020;46(1):39–49. doi: 10.1007/s10695-019-00694-7
  • National Center for Biotechnology Information. National Library of Medicine. NCBI. 2023. Available from: https://www.ncbi.nlm.nih.gov/taxonomy
  • Stroka DM, Burkhardt T, Desbaillets I, et al. HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J. 2001;15(3):2445–2453. doi: 10.1096/fj.01-0125com
  • Chen N, Chen LP, Zhang J, et al. Molecular characterization and expression analysis of three hypoxia-inducible factor alpha subunits, HIF-1α/2α/3α of the hypoxia-sensitive freshwater species, Chinese sucker. Gene. 2012;498(1):81–90. doi: 10.1016/j.gene.2011.12.058
  • Liu S, Zhu K, Chen N, et al. Identification of HIF-1α promoter and expression regulation of HIF-1α gene by LPS and hypoxia in zebrafish. Fish Physiol Biochem. 2013;39(5):1153–1163. doi: 10.1007/s10695-013-9771-0
  • Wang SY, Lau K, Lai KP, et al. Hypoxia causes transgenerational impairments in reproduction of fish. Nat Commun. 2016;7(1):12114. doi: 10.1038/ncomms12114
  • Rahman MS, Thomas P. Molecular cloning, characterization and expression of two hypoxia-inducible factor alpha subunits, HIF-1alpha and HIF-2alpha, in a hypoxia-tolerant marine teleost, Atlantic croaker (Micropogonias undulatus). Gene. 2007;396(2):273–282. doi: 10.1016/j.gene.2007.03.009
  • Wang J, Xu Z, He J. The role of HIF-1α in the energy metabolism and immune responses of hypoxic Scylla paramamosain. Aquacult Rep. 2021;20:100740. doi: 10.1016/j.aqrep.2021.100740
  • Carthew RW, Sontheimer EJ. Origins and mechanisms of miRnas and siRnas. Cell. 2009;136(4):642–655. doi: 10.1016/j.cell.2009.01.035
  • Li C, Zhao M, Zhang C, et al. MiR210 modulates respiratory burst in Apostichopus japonicus coelomocytes via targeting Toll-like receptor. Dev Comp Immunol. 2016;65:377–381. doi: 10.1016/j.dci.2016.08.008
  • Zhang Y, Shao Y, Lv Z, et al. MiR-210 regulates coelomocyte proliferation through targeting E2F3 in Apostichopus japonicus. Fish Shellfish Immunol. 2020;106:83–590. doi: 10.1016/j.fsi.2020.08.036
  • Chen K, Shao Y, Li C. MiR-137 modulates coelomocytes autophagy by targeting Atg13 in the sea cucumber Apostichopus japonicus. Dev Comp Immunol. 2022;135:104486. doi: 10.1016/j.dci.2022.104486
  • Coates CJ, McCulloch C, Betts J, et al. Echinochrome a release by red spherule cells is an iron-withholding strategy of sea urchin innate immunity. J Innate Immun. 2018;10(2):119–130. doi: 10.1159/000484722
  • Palazon A, Goldrath AW, Nizet V, et al. HIF transcription factors, inflammation, and immunity. Immunity. 2014;41(4):518–528. doi: 10.1016/j.immuni.2014.09.008
  • Krzywinska E, Stockmann C. Hypoxia, metabolism and immune cell function. Biomedicines. 2018;6(2):56. doi: 10.3390/biomedicines6020056
  • Lee AH, Ledderose C, Li X, et al. Adenosine triphosphate release is required for toll-like receptor-induced monocyte/macrophage activation, inflammasome signaling, interleukin-1β production, and the host immune response to infection. Crit Care Med. 2018;46(12):e1183–e1189. doi: 10.1097/CCM.0000000000003446
  • Liang Y, Xu ML, Wang XW, et al. ATP synthesis is active on the cell surface of the shrimp Litopenaeus vannamei and is suppressed by WSSV infection. Virol J. 2015;12(1):49. doi: 10.1186/s12985-015-0275-7
  • Courtnay R, Ngo DC, Malik N, et al. Cancer metabolism and the Warburg effect: the role of HIF-1 and PI3K. Mol Biol Rep. 2015;42(4):841–851. doi: 10.1007/s11033-015-3858-x
  • Kierans SJ, Taylor CT. Regulation of glycolysis by the hypoxia-inducible factor (HIF): implications for cellular physiology. J Physiol. 2021;599(1):23–37. doi: 10.1113/JP280572
  • Chen ML, Cheng T, Xu C, et al. Sodium houttuyfonate enhances the mono-therapy of fluconazole on oropharyngeal candidiasis (OPC) through HIF-1α/IL-17 axis by inhibiting cAMP mediated filamentation in Candida albicans-Candida glabrata dual biofilms. Virulence. 2022;13(1):428–443. doi: 10.1080/21505594.2022.2035066
  • Yin X, Peng J, Gu L, et al. Targeting glutamine metabolism in hepatic stellate cells alleviates liver fibrosis. Cell Death Dis. 2022;13(11):955. doi: 10.1038/s41419-022-05409-0
  • Yang S, Zhao J, Cui X, et al. TCA-phospholipid-glycolysis targeted triple therapy effectively suppresses ATP production and tumor growth in glioblastoma. Theranostics. 2022;12(16):7032–7050. doi: 10.7150/thno.74197