The untapped potential of cell culture in disentangling insect-microbial relationships

Christine V. Macpherson , Brendan A. Daisley , Elizabeth Mallory , Emma Allen-Vercoe

Microbiome Research Reports ›› 2024, Vol. 3 ›› Issue (2) : 20

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Microbiome Research Reports ›› 2024, Vol. 3 ›› Issue (2) :20 DOI: 10.20517/mrr.2023.66
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The untapped potential of cell culture in disentangling insect-microbial relationships

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Abstract

Cell culture is a powerful technique for the investigation of molecular mechanisms fundamental to health and disease in a diverse array of organisms. Cell lines offer several advantages, namely their simplistic approach and high degree of reproducibility. One field where cell culture has proven particularly useful is the study of the microbiome, where cell culture has led to the illumination of microbial influences on host immunity, nutrition, and physiology. Thus far, researchers have focused cell culture work predominantly on humans, but the growing field of insect microbiome research stands to benefit greatly from its application. Insects constitute one of Earth’s most diverse and ancient life forms and, just as with humans, possess microbiomes with great significance to their health. Insects, which play critical roles in supporting food security and ecological stability, are facing increasing threats from agricultural intensification, climate change, and pesticide use. As the microbiome is closely tied to host health, gaining a more robust understanding is of increasing importance. In this review, we assert that the cultivation and utilization of insect gut cell lines in microbiome research will bridge critical knowledge gaps essential for informing insect management practices in a world under pressure.

Keywords

Cell culture / host-microbe interactions / insects / gut microbiome

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Christine V. Macpherson, Brendan A. Daisley, Elizabeth Mallory, Emma Allen-Vercoe. The untapped potential of cell culture in disentangling insect-microbial relationships. Microbiome Research Reports, 2024, 3(2): 20 DOI:10.20517/mrr.2023.66

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References

[1]

Segeritz C-P.Chapter 9 - cell culture: growing cells as model systems in vitro. In: Jalali M, Saldanha FYL, Jalali M, editors. Basic science methods for clinical researchers. Boston: Academic Press; 2017. pp. 151-72. PMCID:PMC7149418

[2]

Berg G,Fischer D.Microbiome definition re-visited: old concepts and new challenges.Microbiome2020;8:103 PMCID:PMC7329523

[3]

Lopez-Escalera S.Evaluation of Caco-2 and human intestinal epithelial cells as in vitro models of colonic and small intestinal integrity.Biochem Biophys Rep2022;31:101314 PMCID:PMC9304606

[4]

van Nuenen MHMC, de Ligt RAF, Doornbos RP, van der Woude JCJ, Kuipers EJ, Venema K. The influence of microbial metabolites on human intestinal epithelial cells and macrophages in vitro.FEMS Immunol Med Microbiol2005;45:183-9

[5]

Jahani-Sherafat S,Ghasemian-Safaei H.The effect of intestinal microbiota metabolites on HT29 cell line using MTT method in patients with colorectal cancer.Gastroenterol Hepatol Bed Bench2019;12:S74-9 PMCID:PMC7011068

[6]

Engel P.The gut microbiota of insects - diversity in structure and function.FEMS Microbiol Rev2013;37:699-735

[7]

Jing TZ,Wang ZY.Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?.Microbiome2020;8:38 PMCID:PMC7077154

[8]

Goulson D.The insect apocalypse, and why it matters.Curr Biol2019;29:R967-71

[9]

Janicki J,Scarr S. The collapse of insects. 2022. Available from: https://www.reuters.com/graphics/GLOBAL-ENVIRONMENT/INSECT-APOCALYPSE/egpbykdxjvq/. [Last accessed on 26 Feb 2024]

[10]

Cellosaurus - a knowledge resource on cell lines. Available from: https://www.cellosaurus.org/. [Last accessed on 26 Feb 2024]

[11]

Stork NE.How many species of insects and other terrestrial arthropods are there on earth?.Annu Rev Entomol2018;63:31-45

[12]

Glaser RW.Studies on the wilt disease, or “flacheria” of the gypsy moth.Science1912;36:219-24

[13]

Smagghe G,Stanley D.Insect cell culture and applications to research and pest management.In Vitro Cell Dev Biol Anim2009;45:93-105

[14]

Grace TDC.Establishment of four strains of cells from insect tissues grown in vitro.Nature1962;195:788-9

[15]

Drugmand JC. Characterization of insect cell lines is required for appropriate industrial processes: case study of high-five cells for recombinant protein production. 2007. Available from: https://dial.uclouvain.be/pr/boreal/en/object/boreal%3A4586. [Last accessed on 26 Feb 2024]

[16]

Vaughn JL,Tompkins GJ.The establishment of two cell lines from the insect Spodoptera frugiperda (lepidoptera; noctuidae).In Vitro1977;13:213-7

[17]

Rubio NR,Trimmer BA.Possibilities for engineered insect tissue as a food source.Front Sustain Food Syst2019;3:24

[18]

Gisder S,Linde A.A cell culture model for Nosema ceranae and Nosema apis allows new insights into the life cycle of these important honey bee-pathogenic microsporidia.Environ Microbiol2011;13:404-13

[19]

Goblirsch MJ,Kurtti TJ.A cell line resource derived from honey bee (Apis mellifera) embryonic tissues.PLoS One2013;8:e69831 PMCID:PMC3720946

[20]

Create professional science figures in minutes. BioRender. Available from: https://www.biorender.com/. [Last accessed on 26 Feb 2024]

[21]

Mitsuhashi J.Cell culture of insects. In: Encyclopedia of entomology. Dordrecht: Springer Netherlands; 2005. pp. 480.

[22]

Michl J,Swietach P.Evidence-based guidelines for controlling pH in mammalian live-cell culture systems.Commun Biol2019;2:144 PMCID:PMC6486606

[23]

Singh L,Kumar D.Hypoxia induced lactate acidosis modulates tumor microenvironment and lipid reprogramming to sustain the cancer cell survival.Front Oncol2023;13:1034205 PMCID:PMC9906992

[24]

Warburg O.The metabolism of carcinoma cells.J Cancer Res1925;9:148-63

[25]

Conceição CC,Arcanjo A.Aedes fluviatilis cell lines as new tools to study metabolic and immune interactions in mosquito-Wolbachia symbiosis.Sci Rep2021;11:19202 PMCID:PMC8478883

[26]

Watanabe K,Matsuura Y,Noda H.Intrasperm vertical symbiont transmission.Proc Natl Acad Sci U S A2014;111:7433-7 PMCID:PMC4034255

[27]

Brandt JW,Oliver KM.Culture of an aphid heritable symbiont demonstrates its direct role in defence against parasitoids.Proc Biol Sci2017;284:20171925 PMCID:PMC5698653

[28]

O’Neill SL,Sinkins SP,Andreadis TG.In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line.Insect Mol Biol1997;6:33-9

[29]

Rajagopal R.Beneficial interactions between insects and gut bacteria.Indian J Microbiol2009;49:114-9 PMCID:PMC3450145

[30]

Menezes C,Marsaioli AJ.A Brazilian social bee must cultivate fungus to survive.Curr Biol2015;25:2851-5

[31]

Briones-Roblero CI,Santiago-Cruz JA,Rivera-Orduña FN.Degradation capacities of bacteria and yeasts isolated from the gut of Dendroctonus rhizophagus (Curculionidae: Scolytinae).Folia Microbiol2017;62:1-9

[32]

Gilmore TD.The Rel/NF-κB signal transduction pathway: introduction.Oncogene1999;18:6842-4

[33]

Buchon N,Cherry S.Immunity in Drosophila melanogaster - from microbial recognition to whole-organism physiology.Nat Rev Immunol2014;14:796-810 PMCID:PMC6190593

[34]

Marian B.In vitro models for the identification and characterization of tumor-promoting and protective factors for colon carcinogenesis.Food Chem Toxicol2002;40:1099-104

[35]

Langerholc T,Wollgast J,Cencic A.Novel and established intestinal cell line models - an indispensable tool in food science and nutrition.Trends Food Sci Technol2011;22:S11-20 PMCID:PMC7172287

[36]

Costa J.Advances and current challenges in intestinal in vitro model engineering: a digest.Front Bioeng Biotechnol2019;7:144 PMCID:PMC6591368

[37]

Cencic A.Functional cell models of the gut and their applications in food microbiology - a review.Int J Food Microbiol2010;141:S4-14 PMCID:PMC7173225

[38]

Koczka K,Ernst W,Nika L.Comparative transcriptome analysis of a Trichoplusia ni cell line reveals distinct host responses to intracellular and secreted protein products expressed by recombinant baculoviruses.J Biotechnol2018;270:61-9

[39]

Fu Y,Zhang H.The genome of the Hi5 germ cell line from Trichoplusia ni, an agricultural pest and novel model for small RNA biology.Elife2018;7:e31628 PMCID:PMC5844692

[40]

Wei L,Miao Y.Transcriptome analysis of Spodoptera frugiperda 9 (Sf9) cells infected with baculovirus, AcMNPV or AcMNPV-BmK IT.Biotechnol Lett2017;39:1129-39

[41]

Vorgia E,Denecke S.Functional characterization and transcriptomic profiling of a spheroid-forming midgut cell line from Helicoverpa zea (Lepidoptera: Noctuidae).Insect Biochem Mol Biol2021;128:103510

[42]

Sun H,Liu S,Pang KS.The Caco-2 cell monolayer: usefulness and limitations.Expert Opin Drug Metab Toxicol2008;4:395-411

[43]

Bahrami B,Macfarlane S.Adherence and cytokine induction in Caco-2 cells by bacterial populations from a three-stage continuous-culture model of the large intestine.Appl Environ Microbiol2011;77:2934-42 PMCID:PMC3126424

[44]

Maccaferri S,Brigidi P,Costabile A.Potential probiotic Kluyveromyces marxianus B0399 modulates the immune response in Caco-2 cells and peripheral blood mononuclear cells and impacts the human gut microbiota in an in vitro colonic model system.Appl Environ Microbiol2012;78:956-64 PMCID:PMC3272993

[45]

Castellarin M,Freeman JD.Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma.Genome Res2012;22:299-306 PMCID:PMC3266037

[46]

Dharmani P,Ambrose C,Chadee K.Fusobacterium nucleatum infection of colonic cells stimulates MUC2 mucin and tumor necrosis factor alpha.Infect Immun2011;79:2597-607 PMCID:PMC3191979

[47]

Kleiveland CR.Co-culture Caco-2/immune cells. In: Verhoeckx K, Cotter P, López-Expósito I, et al., editors. The impact of food bioactives on health. Cham: Springer; 2015.

[48]

Lozoya-Agullo I,González-Álvarez I.Usefulness of Caco-2/HT29-MTX and Caco-2/HT29-MTX/Raji B coculture models to predict intestinal and colonic permeability compared to Caco-2 monoculture.Mol Pharm2017;14:1264-70

[49]

Singh D,Arora S,Mahindroo N.Journey of organ on a chip technology and its role in future healthcare scenario.Appl Surf Sci Adv2022;9:100246 PMCID:PMC9000345

[50]

Caccia S,Tettamanti G.The amazing complexity of insect midgut cells: types, peculiarities, and functions.Cell Tissue Res2019;377:505-25

[51]

Dubreuil RR.Copper cells and stomach acid secretion in the Drosophila midgut.Int J Biochem Cell Biol2004;36:745-52

[52]

Wright WE.The two-stage mechanism controlling cellular senescence and immortalization.Exp Gerontol1992;27:383-9

[53]

Namba M,Hyodoh F,Kimoto T.Neoplastic transformation of human diploid fibroblasts (KMST-6) by treatment with 60Co gamma rays.Int J Cancer1985;35:275-80

[54]

Kitagishi Y,Yoshida H,Takahashi J.Long-term cultivation of in vitro Apis mellifera cells by gene transfer of human c-myc proto-oncogene.In Vitro Cell Dev Biol Anim2011;47:451-3

[55]

Bryan TM.SV40-induced immortalization of human cells.Crit Rev Oncog1994;5:331-57

[56]

Zhao Z,Valentine H.Immortalization of human primary prostate epithelial cells via CRISPR inactivation of the CDKN2A locus and expression of telomerase.Prostate Cancer Prostatic Dis2021;24:233-43 PMCID:PMC7917161

[57]

Pringle FM,Goodman CL,Ball LA.Providence virus: a new member of the tetraviridae that infects cultured insect cells.Virology2003;306:359-70

[58]

Kharat KR,Peter S.Development and characterization of new cell line BPH22 from midgut epithelial cells of Poekilocerus pictus (Fabricius, 1775).In Vitro Cell Dev Biol Anim2010;46:824-7

[59]

Granados RR. Cell line isolated from larval midgut tissue of Trichoplusia ni. 1994. Available from: https://patents.google.com/patent/US5298418A/en. [Last accessed on 26 Feb 2024]

[60]

Zhou K,Ringbauer J Jr,Beerntsen B.Establishment of two midgut cell lines from the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae).In Vitro Cell Dev Biol Anim2020;56:10-4

[61]

Abstracts. In vitro cell dev biol anim 1993;29A:30-125A.

[62]

Li J,Yang Y.Establishment and characterization of a novel cell line from midgut tissue of Helicoverpa armigera (Lepidoptera: Noctuidae).In Vitro Cell Dev Biol Anim2015;51:562-71

[63]

Marhoul Z.A mosquito cell line (mos. 55) from Anopheles gambiae larva.Trans R Soc Trop Med Hyg1972;66:183-4

[64]

Aljabr AM,Hussain A,Al-Ayied HY.Establishing midgut cell culture from Rhynchophorus ferrugineus (Olivier) and toxicity assessment against ten different insecticides.In Vitro Cell Dev Biol Anim2014;50:296-303

[65]

Harvey DM.p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts.Genes Dev1991;5:2375-85

[66]

Martorell Ò,Campbell K.Conserved mechanisms of tumorigenesis in the Drosophila adult midgut.PLoS One2014;9:e88413 PMCID:PMC3916428

[67]

Pastor-Pareja JC,Xu T.An innate immune response of blood cells to tumors and tissue damage in Drosophila.Dis Model Mech2008;1:144-54 PMCID:PMC2562178

[68]

Scharrer B.Insect tumors induced by nerve severance: incidence and mortality.Cancer Res1953;13:73-6

[69]

Villegas SN.One hundred years of Drosophila cancer research: no longer in solitude.Dis Model Mech2019;12:dmm039032 PMCID:PMC6505481

[70]

Proto-oncogenes to oncogenes to cancer. Scitable. Available from: https://www.nature.com/scitable/topicpage/proto-oncogenes-to-oncogenes-to-cancer-883/. [Last accessed on 26 Feb 2024]

[71]

Frühauf MI,Botton NY.Alternatives for obtaining a continuous cell line from Apis mellifera.Cienc Rural2021;51:e20201111

[72]

Felgner PL,Holm M.Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure.Proc Natl Acad Sci U S A1987;84:7413-7 PMCID:PMC299306

[73]

Poole CJ.MYC - master regulator of the cancer epigenome and transcriptome.Genes2017;8:142 PMCID:PMC5448016

[74]

Dequéant ML,Hu Y.Discovery of progenitor cell signatures by time-series synexpression analysis during Drosophila embryonic cell immortalization.Proc Natl Acad Sci U S A2015;112:12974-9 PMCID:PMC4620889

[75]

BIRD FT.Tumours associated with a virus infection in an insect.Nature1949;163:777-8

[76]

Kurze C,Dussaubat C.Nosema tolerant honeybees (Apis mellifera) escape parasitic manipulation of apoptosis.PLoS One2015;10:e0140174 PMCID:PMC4596554

[77]

Insect cell lines. Department of Entomology at the University of Kentucky. Available from: https://entomology.ca.uky.edu/aginsectcellsdatabase?combine=&field_cell_order_tid=303&field_cell_species_tid=All&field_cell_stage_tid=All&field_cell_status_tid=All&field_cell_tissue_tid=All. [Last accessed on 26 Feb 2024]

[78]

Sari-Ak D,Shomali RA,Thimiri Govinda Raj DB.Advances in CRISPR-Cas9 for the baculovirus vector system: a systematic review.Viruses2022;15:54 PMCID:PMC9864449

[79]

Nweke EE.Chapter one - development of insect cell line using CRISPR technology. In: Singh V, editor. Progress in molecular biology and translational science.Prog Mol Biol Transl Sci2021;180:1-20

[80]

Carlos-Reyes A,Romero-Garcia S,Hernández-de la Cruz ON.Biological adaptations of tumor cells to radiation therapy.Front Oncol2021;11:718636 PMCID:PMC8652287

[81]

Vaiserman A,Socol Y.Low-dose ionizing radiation as a hormetin: experimental observations and therapeutic perspective for age-related disorders.Biogerontology2021;22:145-64 PMCID:PMC7794644

[82]

Iebba V,Gagliardi A.Eubiosis and dysbiosis: the two sides of the microbiota.New Microbiol2016;39:1-12

[83]

Daisley BA,Engelbrecht K.Emerging connections between gut microbiome bioenergetics and chronic metabolic diseases.Cell Rep2021;37:110087

[84]

Marasco R,Callegari M.Destabilization of the bacterial interactome identifies nutrient restriction-induced dysbiosis in insect guts.Microbiol Spectr2022;10:e0158021 PMCID:PMC8729773

[85]

Tolstoy L. Anna Karenina. The Russian Messenger; 1878.

[86]

Sabree ZL,Arakawa G.Genome shrinkage and loss of nutrient-providing potential in the obligate symbiont of the primitive termite Mastotermes darwiniensis.Appl Environ Microbiol2012;78:204-10 PMCID:PMC3255634

[87]

Su Q,Mu X.Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee.Microbiome2021;9:216 PMCID:PMC8567698

[88]

De Landa GF,Baffoni L.The gut microbiome of solitary bees is mainly affected by pathogen assemblage and partially by land use.Environ Microbiome2023;18:38 PMCID:PMC10131457

[89]

Sender R,Milo R.Revised estimates for the number of human and bacteria cells in the body.PLoS Biol2016;14:e1002533 PMCID:PMC4991899

[90]

Gianetto-Hill CM,Daisley B.The Robogut: a bioreactor model of the human colon for evaluation of gut microbial community ecology and function.Curr Protoc2023;3:e737

[91]

Chevignon G,Brandt JW,Strand MR.Culture-facilitated comparative genomics of the facultative symbiont Hamiltonella defensa.Genome Biol Evol2018;10:786-802 PMCID:PMC5841374

[92]

Zhang Y,Yuan M.Microbiome variation correlates with the insecticide susceptibility in different geographic strains of a significant agricultural pest, Nilaparvata lugens.NPJ Biofilms Microbiomes2023;9:2 PMCID:PMC9837087

[93]

Trinder M,Daisley BA.Probiotic Lactobacillus rhamnosus reduces organophosphate pesticide absorption and toxicity to Drosophila melanogaster.Appl Environ Microbiol2016;82:6204-13 PMCID:PMC5068162

[94]

Leska A,Miśkiewicz K.Binding and detoxification of insecticides by potentially probiotic lactic acid bacteria isolated from honeybee (Apis mellifera L.) environment - an in vitro study.Cells2022;11:3743 PMCID:PMC9740702

[95]

De Weirdt R,Roos S.Glycerol supplementation enhances L. reuteri’s protective effect against S. typhimurium colonization in a 3-D model of colonic epithelium.PLoS One2012;7:e37116 PMCID:PMC3365044

[96]

Daisley BA,Mallory E.Disentangling the microbial ecological factors impacting honey bee susceptibility to Paenibacillus larvae infection.Trends Microbiol2023;31:521-34

[97]

Swevers L,Vogelsang K,Vontas J.Can the mammalian organoid technology be applied to the insect gut?.Pest Manag Sci2021;77:55-63

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