The mechanisms and factors that induce trained immunity in arthropods and mollusks

Besides dividing the organism’s immune system into adaptive and innate immunity, it has long been thought that only adaptive immunity can establish immune memory. However, many studies have shown that innate immunity can also build immunological memory through epigenetic reprogramming and modifications to resist pathogens’ reinfection, known as trained immunity. This paper reviews the role of mitochondrial metabolism and epigenetic modifications and describes the molecular foundation in the trained immunity of arthropods and mollusks. Mitochondrial metabolism and epigenetic modifications complement each other and play a key role in trained immunity.

[1]  B. Igyártó,et al.  Pre-exposure to mRNA-LNP inhibits adaptive immune responses and alters innate immune fitness in an inheritable fashion , 2022, bioRxiv.

[2]  S. Roberts,et al.  Differential DNA methylation in Pacific oyster reproductive tissue in response to ocean acidification , 2022, BMC Genomics.

[3]  N. Fuse,et al.  Genetic dissection of innate immune memory in Drosophila melanogaster , 2022, Frontiers in Immunology.

[4]  Yongfeng Jin,et al.  Trans-splicing facilitated by RNA pairing greatly expands sDscam isoform diversity but not homophilic binding specificity , 2022, Science advances.

[5]  M. Parisi,et al.  Invertebrate Models in Innate Immunity and Tissue Remodeling Research , 2022, International Journal of Molecular Sciences.

[6]  Cang Li,et al.  Metabolomic Investigation of Ultraviolet Ray-Inactivated White Spot Syndrome Virus-Induced Trained Immunity in Marsupenaeus japonicus , 2022, Frontiers in Immunology.

[7]  M. Netea,et al.  Trained immunity: implications for vaccination. , 2022, Current opinion in immunology.

[8]  M. Hussain,et al.  Analysis of Aedes aegypti microRNAs in response to Wolbachia wAlbB infection and their potential role in mosquito longevity , 2022, Scientific Reports.

[9]  G. Sireci,et al.  Metabolic Reprogramming of Innate Immune Cells as a Possible Source of New Therapeutic Approaches in Autoimmunity , 2022, Cells.

[10]  S. Bertrand,et al.  The Evolution of Invertebrate Animals , 2022, Genes.

[11]  C. Chaparro,et al.  Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection , 2022, Microbiome.

[12]  Q. Zeng,et al.  Wolbachia Utilizes lncRNAs to Activate the Anti-Dengue Toll Pathway and Balance Reactive Oxygen Species Stress in Aedes aegypti Through a Competitive Endogenous RNA Network , 2022, Frontiers in Cellular and Infection Microbiology.

[13]  J. Aweya,et al.  Protein Diversity and Immune Specificity of Hemocyanin From Shrimp Litopenaeus vannamei , 2021, Frontiers in Immunology.

[14]  Zhigang Lu,et al.  Receptome profiling identifies KREMEN1 and ASGR1 as alternative functional receptors of SARS-CoV-2 , 2021, Cell research.

[15]  A. Vignal,et al.  Two quantitative trait loci are associated with recapping of Varroa destructor‐infested brood cells in Apis mellifera mellifera , 2021, Animal genetics.

[16]  Zhongwen Xie,et al.  Aspirin Positively Contributes to Drosophila Intestinal Homeostasis and Delays Aging through Targeting Imd , 2021, Aging and disease.

[17]  S. G. Harroun,et al.  Multifunctional carbonized nanogels to treat lethal acute hepatopancreatic necrosis disease , 2021, Journal of Nanobiotechnology.

[18]  K. Brokordt,et al.  Metabolic Cost of the Immune Response During Early Ontogeny of the Scallop Argopecten purpuratus , 2021, Frontiers in Physiology.

[19]  Mark M. Davis,et al.  Systems vaccinology of the BNT162b2 mRNA vaccine in humans , 2021, Nature.

[20]  C. Ke,et al.  Comparative Transcriptome and DNA Methylation Analysis of Phenotypic Plasticity in the Pacific Abalone (Haliotis discus hannai) , 2021, Frontiers in Physiology.

[21]  E. Jeppesen,et al.  Farming practices affect the amino acid profiles of the aquaculture Chinese mitten crab , 2021, PeerJ.

[22]  Mark M. Davis,et al.  The single-cell epigenomic and transcriptional landscape of immunity to influenza vaccination , 2021, Cell.

[23]  Erlend Dancke Sandorf,et al.  Stakeholder perceptions towards sustainable shrimp aquaculture in Vietnam. , 2021, Journal of environmental management.

[24]  R. Tucker,et al.  Did Tenascin-C Co-Evolve With the General Immune System of Vertebrates? , 2021, Frontiers in Immunology.

[25]  Audrey Montigny,et al.  Drosophila primary microRNA-8 encodes a microRNA-encoded peptide acting in parallel of miR-8 , 2021, Genome Biology.

[26]  R. Paul,et al.  Metabolic adjustments during starvation in Daphnia pulex. , 2021, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[27]  T. Mackay,et al.  Functional Diversification, Redundancy, and Epistasis among Paralogs of the Drosophila melanogaster Obp50a–d Gene Cluster , 2021, Molecular biology and evolution.

[28]  M. Vadala',et al.  Immune memory: an evolutionary perspective , 2021, Human vaccines & immunotherapeutics.

[29]  R. Xavier,et al.  Trained immunity, tolerance, priming and differentiation: distinct immunological processes , 2020, Nature Immunology.

[30]  Shikai Liu,et al.  Integrated analysis of microRNA and mRNA expression profiles in Crassostrea gigas to reveal functional miRNA and miRNA-targets regulating shell pigmentation , 2020, Scientific Reports.

[31]  P. David,et al.  The methylome of Biomphalaria glabrata and other mollusks: enduring modification of epigenetic landscape and phenotypic traits by a new DNA methylation inhibitor , 2020, Epigenetics & Chromatin.

[32]  A. Whitehead,et al.  Evolved differences in energy metabolism and growth dictate the impacts of ocean acidification on abalone aquaculture , 2020, Proceedings of the National Academy of Sciences.

[33]  Albertha J. M. Walhout,et al.  Modeling tissue‐relevant Caenorhabditis elegans metabolism at network, pathway, reaction, and metabolite levels , 2020, Molecular systems biology.

[34]  M. Song,et al.  Cross-Protection against MERS-CoV by Prime-Boost Vaccination Using Viral Spike DNA and Protein , 2020, Journal of Virology.

[35]  A. Calixto,et al.  Intergenerational Pathogen-Induced Diapause in Caenorhabditis elegans Is Modulated by mir-243 , 2020, mBio.

[36]  Wei Wang,et al.  DNA methylation mediates differentiation in thermal responses of Pacific oyster (Crassostrea gigas) derived from different tidal levels , 2020, Heredity.

[37]  N. Gerardo,et al.  Evolution of animal immunity in the light of beneficial symbioses , 2020, Philosophical Transactions of the Royal Society B.

[38]  Haihui Ye,et al.  Transcriptional Inhibition of Sp-IAG by Crustacean Female Sex Hormone in the Mud Crab, Scylla paramamosain , 2020, International journal of molecular sciences.

[39]  V. Russo,et al.  Novel Food-Based Product Communication: A Neurophysiological Study , 2020, Nutrients.

[40]  M. Netea,et al.  Maternal Priming: Bacillus Calmette-Guérin (BCG) Vaccine Scarring in Mothers Enhances the Survival of Their Child With a BCG Vaccine Scar. , 2020, Journal of the Pediatric Infectious Diseases Society.

[41]  Jun Wang,et al.  Air Exposure Affects Physiological Responses, Innate Immunity, Apoptosis and DNA Methylation of Kuruma Shrimp, Marsupenaeus japonicus , 2020, Frontiers in Physiology.

[42]  C. Chaparro,et al.  A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas , 2020, mBio.

[43]  R. Xavier,et al.  Defining trained immunity and its role in health and disease , 2020, Nature Reviews Immunology.

[44]  Ali Ali,et al.  Re-thinking adaptive immunity in the beetles: Evolutionary and functional trajectories of lncRNAs. , 2020, Genomics.

[45]  P. David,et al.  Epigenetic inheritance and intergenerational effects in mollusks. , 2020, Gene.

[46]  U. Dobrindt,et al.  MicroRNAs regulate innate immunity against uropathogenic and commensal-like Escherichia coli infections in the surrogate insect model Galleria mellonella , 2020, Scientific Reports.

[47]  N. Chandel,et al.  Mitochondrial TCA cycle metabolites control physiology and disease , 2020, Nature Communications.

[48]  A. Peña‐Rodríguez,et al.  White spot syndrome virus down-regulates expression of histones H2A and H4 of Penaeus vannamei to promote viral replication. , 2019, Diseases of aquatic organisms.

[49]  Z. Cai,et al.  Study of metabolic disorders associated with BDE-47 exposure in Drosophila model by MS-based metabolomics. , 2019, Ecotoxicology and environmental safety.

[50]  D. Vanrompay,et al.  Phloroglucinol Treatment Induces Transgenerational Epigenetic Inherited Resistance Against Vibrio Infections and Thermal Stress in a Brine Shrimp (Artemia franciscana) Model , 2019, Front. Immunol..

[51]  R. Sridharan,et al.  Coordinated removal of repressive epigenetic modifications during induced reversal of cell identity , 2019, The EMBO journal.

[52]  M. Vainstein,et al.  Genome-wide DNA methylation analysis of Metarhizium anisopliae during tick mimicked infection condition , 2019, BMC Genomics.

[53]  Weidong Zhu,et al.  Mechanisms and Functions of Long Non-Coding RNAs at Multiple Regulatory Levels , 2019, International journal of molecular sciences.

[54]  Robert J. Schmitz,et al.  DNA Methylation: Shared and Divergent Features across Eukaryotes. , 2019, Trends in genetics : TIG.

[55]  C. Handschin,et al.  How Epigenetic Modifications Drive the Expression and Mediate the Action of PGC-1α in the Regulation of Metabolism , 2019, International journal of molecular sciences.

[56]  Cheng-Han Wu,et al.  Cross-Talk between Mitochondrial Dysfunction-Provoked Oxidative Stress and Aberrant Noncoding RNA Expression in the Pathogenesis and Pathophysiology of SLE , 2019, International journal of molecular sciences.

[57]  S. Asgari,et al.  Induction of DNA methyltransferase genes in Helicoverpa armigera following injection of pathogenic bacteria modulates expression of antimicrobial peptides and affects bacterial proliferation. , 2019, Journal of insect physiology.

[58]  Yue Wang,et al.  SpBark Suppresses Bacterial Infection by Mediating Hemocyte Phagocytosis in an Invertebrate Model, Scylla paramamosain , 2019, Front. Immunol..

[59]  B. Degnan,et al.  Convergent evolution of a vertebrate-like methylome in a marine sponge , 2019, Nature Ecology & Evolution.

[60]  Youji Wang,et al.  Differential in vivo hemocyte responses to nano titanium dioxide in mussels: Effects of particle size. , 2019, Aquatic toxicology.

[61]  J. Aweya,et al.  Analysis of Litopenaeus vannamei hemocyanin interacting proteins reveals its role in hemolymph clotting. , 2019, Journal of proteomics.

[62]  Rebecca S. Moore,et al.  Piwi/PRG-1 Argonaute and TGF-β Mediate Transgenerational Learned Pathogenic Avoidance , 2019, Cell.

[63]  L. Smith,et al.  Individual Sea Urchin Coelomocytes Undergo Somatic Immune Gene Diversification , 2019, Front. Immunol..

[64]  Jun Wan,et al.  An all-to-all approach to the identification of sequence-specific readers for epigenetic DNA modifications on cytosine , 2019, Nature Communications.

[65]  Yawen Bai,et al.  Chromatin structures condensed by linker histones. , 2019, Essays in biochemistry.

[66]  V. Suárez-Ulloa,et al.  Seasonal DNA Methylation Variation in the Flat Tree Oyster Isognomon Alatus from a Mangrove Ecosystem in North Biscayne Bay, Florida , 2019, Journal of Shellfish Research.

[67]  S. Cowley,et al.  Acetylation & Co: an expanding repertoire of histone acylations regulates chromatin and transcription , 2019, Essays in biochemistry.

[68]  R. DaMatta,et al.  Alterations in the Mitochondrial Physiology of Biomphalaria glabrata (Mollusca: Gastropoda) After Experimental Infection by Angiostrongylus cantonensis (Nematoda: Metastrongylidae) , 2019, Acta Parasitologica.

[69]  A. Kirmizis,et al.  Histone Modifications as an Intersection Between Diet and Longevity , 2019, Front. Genet..

[70]  A. Vilcinskas,et al.  Epigenetic Mechanisms Are Involved in Sex-Specific Trans-Generational Immune Priming in the Lepidopteran Model Host Manduca sexta , 2019, Front. Physiol..

[71]  A. Rao,et al.  TET Enzymes and 5hmC in Adaptive and Innate Immune Systems , 2019, Front. Immunol..

[72]  J. Aweya,et al.  Litopenaeus vannamei attenuates white spot syndrome virus replication by specific antiviral peptides generated from hemocyanin , 2019, Developmental and comparative immunology.

[73]  Ximing Guo,et al.  Transgenerational plasticity and antiviral immunity in the Pacific oyster (Crassostrea gigas) against Ostreid herpesvirus 1 (OsHV‐1) , 2019, Developmental and comparative immunology.

[74]  L. Joosten,et al.  Induction of innate immune memory: the role of cellular metabolism. , 2019, Current opinion in immunology.

[75]  M. Drancourt,et al.  Trained Immunity Carried by Non-immune Cells , 2019, Front. Microbiol..

[76]  L. Joosten,et al.  Innate and Adaptive Immune Memory: an Evolutionary Continuum in the Host's Response to Pathogens. , 2019, Cell host & microbe.

[77]  M. Netea,et al.  DNA Synthesis Is Activated in Mosquitoes and Human Monocytes During the Induction of Innate Immune Memory , 2018, Front. Immunol..

[78]  G. Ratnaparkhi,et al.  Drosophila DNA/RNA methyltransferase contributes to robust host defense in aging animals by regulating sphingolipid metabolism , 2018, Journal of Experimental Biology.

[79]  J. Schertzer,et al.  Induction of Autonomous Memory Alveolar Macrophages Requires T Cell Help and Is Critical to Trained Immunity , 2018, Cell.

[80]  Muhammad Amir Yunus,et al.  Systematic identification and characterization of Aedes aegypti long noncoding RNAs (lncRNAs) , 2018, Scientific Reports.

[81]  R. Godfrey,et al.  Altered Cellular Metabolism Drives Trained Immunity , 2018, Trends in Endocrinology & Metabolism.

[82]  D. E. de Almeida Nagata,et al.  Notch ligand Delta-like 4 induces epigenetic regulation of Treg cell differentiation and function in viral infection , 2018, Mucosal Immunology.

[83]  M. Netea,et al.  Innate immune memory: An evolutionary perspective , 2018, Immunological reviews.

[84]  H. Wang,et al.  What vaccination studies tell us about immunological memory within the innate immune system of cultured shrimp and crayfish. , 2018, Developmental and comparative immunology.

[85]  J. Aweya,et al.  Trypsin of Litopenaeus vannamei is required for the generation of hemocyanin‐derived peptides , 2018, Developmental and comparative immunology.

[86]  Y. Wang,et al.  Histone Modifications in Aging: The Underlying Mechanisms and Implications. , 2018, Current stem cell research & therapy.

[87]  J. Mendell,et al.  Functional Classification and Experimental Dissection of Long Noncoding RNAs , 2018, Cell.

[88]  L. Joosten,et al.  Modulation of Myelopoiesis Progenitors Is an Integral Component of Trained Immunity , 2018, Cell.

[89]  Irah L. King,et al.  BCG Educates Hematopoietic Stem Cells to Generate Protective Innate Immunity against Tuberculosis , 2018, Cell.

[90]  M. Oosting,et al.  Western Diet Triggers NLRP3-Dependent Innate Immune Reprogramming , 2018, Cell.

[91]  J. Aweya,et al.  Glycosylation of hemocyanin in Litopenaeus vannamei is an antibacterial response feature. , 2017, Immunology letters.

[92]  Wencai Jie,et al.  DNA methylation in silkworm genome may provide insights into epigenetic regulation of response to Bombyx mori cypovirus infection , 2017, Scientific Reports.

[93]  Caren Weinhouse Mitochondrial-epigenetic crosstalk in environmental toxicology. , 2017, Toxicology.

[94]  Mark W. Smithson,et al.  Epigenetics and adaptive phenotypic variation between habitats in an asexual snail , 2017, Scientific Reports.

[95]  M. Pauletto,et al.  Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas , 2017, Scientific Reports.

[96]  N. F. D. de Oliveira,et al.  Perkinsus infection is associated with alterations in the level of global DNA methylation of gills and gastrointestinal tract of the oyster Crassostrea gasar. , 2017, Journal of invertebrate pathology.

[97]  Xiao Liu,et al.  Effects of temperature and salinity on survival, growth and DNA methylation of juvenile Pacific abalone, Haliotis discus hannai Ino , 2017, Chinese Journal of Oceanology and Limnology.

[98]  B. Christensen,et al.  Cell-type deconvolution from DNA methylation: a review of recent applications , 2017, Human molecular genetics.

[99]  Yueling Zhang,et al.  C-Terminal Domain of Hemocyanin, a Major Antimicrobial Protein from Litopenaeus vannamei: Structural Homology with Immunoglobulins and Molecular Diversity , 2017, Front. Immunol..

[100]  J. Auwerx,et al.  Mitochondria and Epigenetics - Crosstalk in Homeostasis and Stress. , 2017, Trends in cell biology.

[101]  G. Vassalli,et al.  Exosomes: Therapy delivery tools and biomarkers of diseases , 2017, Pharmacology & therapeutics.

[102]  R. Hardy,et al.  Wolbachia elevates host methyltransferase expression to block an RNA virus early during infection , 2017, PLoS pathogens.

[103]  Costanza Emanueli,et al.  Transcriptional and Post-transcriptional Gene Regulation by Long Non-coding RNA , 2017, Genom. Proteom. Bioinform..

[104]  Kathrin K. Geyer,et al.  The Biomphalaria glabrata DNA methylation machinery displays spatial tissue expression, is differentially active in distinct snail populations and is modulated by interactions with Schistosoma mansoni , 2017, PLoS neglected tropical diseases.

[105]  V. Suárez-Ulloa,et al.  Effects of Florida Red Tides on histone variant expression and DNA methylation in the Eastern oyster Crassostrea virginica. , 2017, Aquatic toxicology.

[106]  M. Helm,et al.  Comprehensive DNA methylation analysis of the Aedes aegypti genome , 2016, Scientific Reports.

[107]  Scott B. Crown,et al.  Lipids Reprogram Metabolism to Become a Major Carbon Source for Histone Acetylation. , 2016, Cell reports.

[108]  Christian M. Metallo,et al.  ATP-Citrate Lyase Controls a Glucose-to-Acetate Metabolic Switch. , 2016, Cell reports.

[109]  L. Joosten,et al.  Immunometabolic circuits in trained immunity. , 2016, Seminars in immunology.

[110]  A. C. Morandini,et al.  Role of epigenetics in modulation of immune response at the junction of host-pathogen interaction and danger molecule signaling. , 2016, Pathogens and disease.

[111]  Yueling Zhang,et al.  Evidences of abundant hemocyanin variants in shrimp Litopenaeus vannamei. , 2016, Molecular immunology.

[112]  Yueling Zhang,et al.  Identification and characterization of an 18.4kDa antimicrobial truncation from shrimp Litopenaeus vannamei hemocyanin upon Vibrio parahaemolyticus infection. , 2016, Fish & shellfish immunology.

[113]  H. Decker,et al.  Immunological properties of oxygen-transport proteins: hemoglobin, hemocyanin and hemerythrin , 2016, Cellular and Molecular Life Sciences.

[114]  Barbara Milutinović,et al.  Immune memory in invertebrates. , 2016, Seminars in immunology.

[115]  J. Tyler,et al.  Epigenetics and aging , 2016, Science Advances.

[116]  Ian C. McDowell,et al.  Multi-species protein similarity clustering reveals novel expanded immune gene families in the eastern oyster Crassostrea virginica. , 2016, Fish & shellfish immunology.

[117]  I. Söderhäll,et al.  Retraction: Bacteria-Induced Dscam Isoforms of the Crustacean, Pacifastacus leniusculus , 2016, PLoS pathogens.

[118]  R. Xavier,et al.  Trained immunity: A program of innate immune memory in health and disease , 2016, Science.

[119]  L. B. Snoek,et al.  Contrasting invertebrate immune defense behaviors caused by a single gene, the Caenorhabditis elegans neuropeptide receptor gene npr-1 , 2016, BMC Genomics.

[120]  D. Vanrompay,et al.  Probing the phenomenon of trained immunity in invertebrates during a transgenerational study, using brine shrimp Artemia as a model system , 2016, Scientific Reports.

[121]  E. Jablonka,et al.  Editorial: Epigenetics as a Deep Intimate Dialogue between Host and Symbionts , 2016, Front. Genet..

[122]  N. Pujol,et al.  Local and long-range activation of innate immunity by infection and damage in C. elegans. , 2016, Current opinion in immunology.

[123]  M. Netea,et al.  Immunological memory: lessons from the past and a look to the future , 2016, Nature Reviews Immunology.

[124]  R. Deberardinis,et al.  TCA Cycle and Mitochondrial Membrane Potential Are Necessary for Diverse Biological Functions. , 2016, Molecular cell.

[125]  N. Dheilly,et al.  A Shift from Cellular to Humoral Responses Contributes to Innate Immune Memory in the Vector Snail Biomphalaria glabrata , 2016, PLoS pathogens.

[126]  Wentao Yang,et al.  High Innate Immune Specificity through Diversified C-Type Lectin-Like Domain Proteins in Invertebrates , 2015, Journal of Innate Immunity.

[127]  C. Handschin,et al.  Complex Coordination of Cell Plasticity by a PGC-1α-controlled Transcriptional Network in Skeletal Muscle , 2015, Front. Physiol..

[128]  L. Smith,et al.  Extraordinary Diversity of Immune Response Proteins among Sea Urchins: Nickel-Isolated Sp185/333 Proteins Show Broad Variations in Size and Charge , 2015, PloS one.

[129]  U. Conrath,et al.  Priming for enhanced defense. , 2015, Annual review of phytopathology.

[130]  N. Chandel Evolution of Mitochondria as Signaling Organelles. , 2015, Cell metabolism.

[131]  J. Ruas,et al.  The hitchhiker’s guide to PGC-1α isoform structure and biological functions , 2015, Diabetologia.

[132]  Xiaolong Hu,et al.  The gene expression profile of resistant and susceptible Bombyx mori strains reveals cypovirus-associated variations in host gene transcript levels , 2015, Applied Microbiology and Biotechnology.

[133]  G. Litman,et al.  Massive expansion and functional divergence of innate immune genes in a protostome , 2015, Scientific Reports.

[134]  S. Shen-Orr,et al.  Glycolysis-mediated changes in acetyl-CoA and histone acetylation control the early differentiation of embryonic stem cells. , 2015, Cell metabolism.

[135]  T. Tylleskär,et al.  Child survival and BCG vaccination: a community based prospective cohort study in Uganda , 2015, BMC Public Health.

[136]  B. Tu,et al.  Acetyl-CoA and the Regulation of Metabolism: Mechanisms and Consequences , 2015, Current opinion in cell biology.

[137]  P. Bossier,et al.  Multigenerational immune priming in an invertebrate parthenogenetic Artemia to a pathogenic Vibrio campbellii. , 2015, Fish & shellfish immunology.

[138]  S. Degnan The surprisingly complex immune gene repertoire of a simple sponge, exemplified by the NLR genes: a capacity for specificity? , 2015, Developmental and comparative immunology.

[139]  S. Bordenstein,et al.  Distributed under Creative Commons Cc-by 4.0 the Relative Importance of Dna Methylation and Dnmt2-mediated Epigenetic Regulation on Wolbachia Densities and Cytoplasmic Incompatibility , 2022 .

[140]  R. Klose,et al.  Understanding the relationship between DNA methylation and histone lysine methylation , 2014, Biochimica et biophysica acta.

[141]  P. Sorgeloos,et al.  Reactive oxygen species generated by a heat shock protein (Hsp) inducing product contributes to Hsp70 production and Hsp70-mediated protective immunity in Artemia franciscana against pathogenic vibrios. , 2014, Developmental and comparative immunology.

[142]  R. Xavier,et al.  Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity , 2014, Science.

[143]  Ian A Blair,et al.  Akt-dependent metabolic reprogramming regulates tumor cell histone acetylation. , 2014, Cell metabolism.

[144]  Keith W. Vance,et al.  Transcriptional regulatory functions of nuclear long noncoding RNAs , 2014, Trends in genetics : TIG.

[145]  M. Vandegehuchte,et al.  Environmental heat stress induces epigenetic transgenerational inheritance of robustness in parthenogenetic Artemia model , 2014, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[146]  M. Netea,et al.  Innate immune memory: towards a better understanding of host defense mechanisms. , 2014, Current opinion in immunology.

[147]  Harri Lähdesmäki,et al.  Dissecting the dynamic changes of 5-hydroxymethylcytosine in T-cell development and differentiation , 2014, Proceedings of the National Academy of Sciences.

[148]  Lingling Wang,et al.  The specifically enhanced cellular immune responses in Pacific oyster (Crassostrea gigas) against secondary challenge with Vibrio splendidus. , 2014, Developmental and comparative immunology.

[149]  Richa,et al.  Hydroxymethylation of DNA , 2014 .

[150]  Kun Gao,et al.  Cytoplasmic polyhedrosis virus-induced differential gene expression in two silkworm strains of different susceptibility. , 2014, Gene.

[151]  A. Chawla,et al.  Metabolic regulation of immune responses. , 2014, Annual review of immunology.

[152]  A. Vilcinskas,et al.  The maternal transfer of bacteria can mediate trans-generational immune priming in insects , 2014, Virulence.

[153]  Gordon D. Brown,et al.  Signalling C‐Type lectin receptors, microbial recognition and immunity , 2014, Cellular microbiology.

[154]  Yueling Zhang,et al.  Evidences of SNPs in the variable region of hemocyanin Ig-like domain in shrimp Litopenaeus vannamei. , 2013, Fish & shellfish immunology.

[155]  Christine G. Elsik,et al.  RNA interference knockdown of DNA methyl-transferase 3 affects gene alternative splicing in the honey bee , 2013, Proceedings of the National Academy of Sciences.

[156]  S. Asgari,et al.  Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti , 2013, Proceedings of the National Academy of Sciences.

[157]  Xinnian Dong,et al.  Systemic acquired resistance: turning local infection into global defense. , 2013, Annual review of plant biology.

[158]  S. Cherry,et al.  Efficient RNA virus control in Drosophila requires the RNA methyltransferase Dnmt2 , 2013, EMBO reports.

[159]  P. Potter One Rotten Apple Infects All in the Basket , 2013, Emerging Infectious Diseases.

[160]  R. Chandra,et al.  Anopheles NF-κB-regulated splicing factors direct pathogen-specific repertoires of the hypervariable pattern recognition receptor AgDscam. , 2012, Cell host & microbe.

[161]  R. Fischer,et al.  Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection , 2012, Frontiers in Zoology.

[162]  R. Xavier,et al.  Bacille Calmette-Guérin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes , 2012, Proceedings of the National Academy of Sciences.

[163]  Yueling Zhang,et al.  SNPs of hemocyanin C‐terminal fragment in shrimp Litopenaeus vannamei , 2012, FEBS letters.

[164]  B. Ramsahoye,et al.  Lactate, a product of glycolytic metabolism, inhibits histone deacetylase activity and promotes changes in gene expression , 2012, Nucleic acids research.

[165]  A. Zibaee,et al.  Cellular Immune Reactions of the Sunn Pest, Eurygaster integriceps, to the Entomopathogenic Fungus, Beauveria bassiana and Its Secondary Metabolites , 2011, Journal of insect science.

[166]  W. Marston Linehan,et al.  Reductive carboxylation supports growth in tumor cells with defective mitochondria , 2011, Nature.

[167]  R. Ley,et al.  The Antibacterial Lectin RegIIIγ Promotes the Spatial Segregation of Microbiota and Host in the Intestine , 2011, Science.

[168]  Xiaobo Zhang,et al.  Contribution of the Caspase Gene Sequence Diversification to the Specifically Antiviral Defense in Invertebrate , 2011, PloS one.

[169]  H. Blau,et al.  DNA Demethylation Dynamics , 2011, Cell.

[170]  L. Smith,et al.  Invertebrate immune diversity. , 2011, Developmental and comparative immunology.

[171]  S. Asgari Role of MicroRNAs in Insect Host–Microorganism Interactions , 2011, Front. Physio..

[172]  Keith D Robertson,et al.  DNA methylation: superior or subordinate in the epigenetic hierarchy? , 2011, Genes & cancer.

[173]  M. Netea,et al.  Trained immunity: a memory for innate host defense. , 2011, Cell host & microbe.

[174]  R. Maleszka,et al.  Insects as innovative models for functional studies of DNA methylation. , 2011, Trends in genetics : TIG.

[175]  A. Pedersen,et al.  Within and transgenerational immune priming in an insect to a DNA virus , 2011, Proceedings of the Royal Society B: Biological Sciences.

[176]  Andrew J. Bannister,et al.  Regulation of chromatin by histone modifications , 2011, Cell Research.

[177]  W. Reik,et al.  Epigenetic Reprogramming in Plant and Animal Development , 2010, Science.

[178]  C. Barillas-Mury,et al.  Hemocyte Differentiation Mediates Innate Immune Memory in Anopheles gambiae Mosquitoes , 2010, Science.

[179]  Yves Moné,et al.  A Large Repertoire of Parasite Epitopes Matched by a Large Repertoire of Host Immune Receptors in an Invertebrate Host/Parasite Model , 2010, PLoS neglected tropical diseases.

[180]  M. .. Alvarez,et al.  Epigenetic control of plant immunity. , 2010, Molecular plant pathology.

[181]  K. Kristiansen,et al.  Single base–resolution methylome of the silkworm reveals a sparse epigenomic map , 2010, Nature Biotechnology.

[182]  J. J. Jansen,et al.  Stress-induced DNA methylation changes and their heritability in asexual dandelions. , 2010, The New phytologist.

[183]  P. Schmid-Hempel,et al.  Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. , 2010, The Journal of animal ecology.

[184]  Chase A. Miller,et al.  Sp185/333: a novel family of genes and proteins involved in the purple sea urchin immune response. , 2010, Developmental and comparative immunology.

[185]  D. Heckel,et al.  Dietary-dependent trans-generational immune priming in an insect herbivore , 2009, Proceedings of the Royal Society B: Biological Sciences.

[186]  J. Xiang,et al.  Molecular cloning and characterisation of prophenoloxidase (ProPO) cDNA from Fenneropenaeus chinensis and its transcription injected by Vibrio anguillarum , 2009, Molecular Biology Reports.

[187]  F. Kafatos,et al.  Two C-type Lectins Cooperate to Defend Anopheles gambiae against Gram-negative Bacteria* , 2009, The Journal of Biological Chemistry.

[188]  P. Schmid-Hempel,et al.  Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum , 2009, Proceedings of the Royal Society B: Biological Sciences.

[189]  K. Morris,et al.  The Dscam homologue of the crustacean Daphnia is diversified by alternative splicing like in insects. , 2008, Molecular biology and evolution.

[190]  A. Bird,et al.  DNA methylation landscapes: provocative insights from epigenomics , 2008, Nature Reviews Genetics.

[191]  L. Smith,et al.  Localization and diversity of 185/333 proteins from the purple sea urchin – unexpected protein-size range and protein expression in a new coelomocyte type , 2008, Journal of Cell Science.

[192]  A. Xu,et al.  A Short-Form C-Type Lectin from Amphioxus Acts as a Direct Microbial Killing Protein via Interaction with Peptidoglycan and Glucan1 , 2007, The Journal of Immunology.

[193]  H. Schulenburg,et al.  How do invertebrates generate a highly specific innate immune response? , 2007, Molecular immunology.

[194]  Xiao-qiang Yu,et al.  Drosophila C-type lectins enhance cellular encapsulation. , 2007, Molecular immunology.

[195]  Katherine M. Buckley,et al.  The immune gene repertoire encoded in the purple sea urchin genome. , 2006, Developmental biology.

[196]  Kenjiro Ueda,et al.  Characterization of a Novel C-Type Lectin, Bombyx mori Multibinding Protein, from the B. mori Hemolymph: Mechanism of Wide-Range Microorganism Recognition and Role in Immunity1 , 2006, The Journal of Immunology.

[197]  P. Schmid-Hempel,et al.  Insect Immunity Shows Specificity in Protection upon Secondary Pathogen Exposure , 2006, Current Biology.

[198]  H. Taylor,et al.  AgDscam, a Hypervariable Immunoglobulin Domain-Containing Receptor of the Anopheles gambiae Innate Immune System , 2006, PLoS biology.

[199]  S. Natori,et al.  Participation of a galactose-specific C-type lectin in Drosophila immunity. , 2006, The Biochemical journal.

[200]  L. Pasquier Germline and somatic diversification of immune recognition elements in Metazoa. , 2006, Immunology letters.

[201]  M. Cooper,et al.  The Evolution of Adaptive Immune Systems , 2006, Cell.

[202]  M. Kondo,et al.  Extensive Diversity of Ig-Superfamily Proteins in the Immune System of Insects , 2005, Science.

[203]  D. Hultmark,et al.  Invertebrate immunity and the limits of mechanistic immunology , 2005, Nature Immunology.

[204]  Joachim Kurtz,et al.  Specific memory within innate immune systems. , 2005, Trends in immunology.

[205]  Ana Marija Hošnjak,et al.  ORIGINAL PAPER , 1996 .

[206]  T. Kepler,et al.  Invertebrate immune systems – not homogeneous, not simple, not well understood , 2004, Immunological reviews.

[207]  Xiao-qiang Yu,et al.  Innate immune responses of a lepidopteran insect, Manduca sexta , 2004, Immunological reviews.

[208]  J. Kurtz,et al.  Innate defence: Evidence for memory in invertebrate immunity , 2003, Nature.

[209]  G. Storz An Expanding Universe of Noncoding RNAs , 2002, Science.

[210]  Guillaume Adelmant,et al.  Activation of PPARγ coactivator-1 through transcription factor docking , 1999 .

[211]  B. Lemaître,et al.  Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[212]  P. Puccetti,et al.  Evidence for macrophage-mediated protection against lethal Candida albicans infection , 1986, Infection and immunity.

[213]  OUP accepted manuscript , 2022, Journal of Insect Science.

[214]  Li-Fang Hu Epigenetic Regulation of Autophagy. , 2019, Advances in experimental medicine and biology.

[215]  S. Sivanand,et al.  Spatiotemporal Control of Acetyl-CoA Metabolism in Chromatin Regulation. , 2018, Trends in biochemical sciences.

[216]  N. Debattista,et al.  Natural Food Preservatives Against Microorganisms , 2018 .

[217]  Johan Auwerx,et al.  Protein acetylation in metabolism — metabolites and cofactors , 2016, Nature Reviews Endocrinology.

[218]  M. Netea,et al.  Trained immunity: consequences for the heterologous effects of BCG vaccination. , 2015, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[219]  Z. Hevesi,et al.  Anesthesia care for liver transplantation. , 2011, Transplantation reviews.

[220]  Yueling Zhang,et al.  Identification and agglutination properties of hemocyanin from the mud crab (Scylla serrata). , 2011, Fish & shellfish immunology.

[221]  Ting Liu,et al.  Microarray analysis of the gene expression profile in the midgut of silkworm infected with cytoplasmic polyhedrosis virus , 2010, Molecular Biology Reports.

[222]  Darren J Obbard,et al.  Explorer Alternative splicing of the Anopheles gambiae Dscam gene in diverse Plasmodium falciparum infections , 2017 .

[223]  Identification and characterization of glycosylation sites on Litopenaeus vannamei hemocyanin , 2022 .