Skip to main content

A Light in the Dark: Uncovering Wolbachia-Host Interactions Using Fluorescence Imaging

  • Protocol
  • First Online:
Wolbachia

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2739))

Abstract

The success of microbial endosymbionts, which reside naturally within a eukaryotic “host” organism, requires effective microbial interaction with, and manipulation of, the host cells. Fluorescence microscopy has played a key role in elucidating the molecular mechanisms of endosymbiosis. For 30 years, fluorescence analyses have been a cornerstone in studies of endosymbiotic Wolbachia bacteria, focused on host colonization, maternal transmission, reproductive parasitism, horizontal gene transfer, viral suppression, and metabolic interactions in arthropods and nematodes. Fluorescence-based studies stand to continue informing Wolbachia-host interactions in increasingly detailed and innovative ways.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Landmann F (2019) The Wolbachia endosymbionts. Microbiol Spectr 7 (2):BAI-0018-2019. https://doi.org/10.1128/microbiolspec.BAI-0018-2019

  2. Hertig M, Wolbach SB (1924) Studies on Rickettsia-like micro-organisms in insects. J Med Res 44(3):329–374.327

    Google Scholar 

  3. Fallon AM (2008) Cytological properties of an Aedes albopictus mosquito cell line infected with Wolbachia strain wAlbB. In Vitro Cell Dev Biol Anim 44(5–6):154–161. https://doi.org/10.1007/s11626-008-9090-4

  4. Muniaraj M, Paramasivan R, Sunish IP et al (2012) Detection of Wolbachia endobacteria in Culex quinquefasciatus by Gimenez staining and confirmation by PCR. J Vector Borne Dis 49(4):258–261

    Google Scholar 

  5. Fenollar F, La Scola B, Inokuma H et al (2003) Culture and phenotypic characterization of a Wolbachia pipientis isolate. J Clin Microbiol 41(12):5434–5441. https://doi.org/10.1128/jcm.41.12.5434-5441.2003

  6. Breeuwer JA, Werren JH (1990) Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346(6284):558–560. https://doi.org/10.1038/346558a0

    Article  CAS  PubMed  Google Scholar 

  7. Stouthamer R, Werren JH (1993) Microbes associated with parthenogenesis in wasps of the genus Trichogramma. Jour Invert Pathol 61(1):6–9

    Article  Google Scholar 

  8. Strunov A, Kiseleva E (2016) Drosophila melanogaster brain invasion: pathogenic Wolbachia in central nervous system of the fly. Insect Sci 23(2):253–264. https://doi.org/10.1111/1744-7917.12187

  9. Szollosi A, Debec A (1980) Presence of Rickettsias in Haploid Drosophila melanogaster. Cell Lines 38:129–134

    Google Scholar 

  10. Fischer K, Beatty WL, Weil GJ et al (2014) High pressure freezing/freeze substitution fixation improves the ultrastructural assessment of Wolbachia endosymbiont-filarial nematode host interaction. PLoS One 9(1):e86383. https://doi.org/10.1371/journal.pone.0086383

  11. O’Neill SL, Pettigrew MM, Sinkins SP et al (1997) In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line. Insect Mol Biol 6(1):33–39. https://doi.org/10.1046/j.1365-2583.1997.00157.x

    Article  PubMed  Google Scholar 

  12. Chagas-Moutinho VA, Silva R, de Souza W, Machado Motta MC (2015) Identification and ultrastructural characterization of the Wolbachia symbiont in Litomosoides chagasfilhoi. Parasites Vectors 8(74). https://doi.org/10.1186/s13071-015-0668-x

  13. White PM, Pietri JE, Debec A et al (2017) Mechanisms of horizontal cell-to-cell transfer of Wolbachia spp. in Drosophila melanogaster. Appl Environ Microbiol 83(7). https://doi.org/10.1128/aem.03425-16

  14. Voronin D, Guimarães AF, Molyneux GR et al (2014) Wolbachia lipoproteins: abundance, localisation and serology of Wolbachia peptidoglycan associated lipoprotein and the type IV secretion system component, VirB6 from Brugia malayi and Aedes albopictus. Parasit Vectors 7:462. https://doi.org/10.1186/s13071-014-0462-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kramer LH, Passeri B, Corona S et al (2003) Immunohistochemical/immunogold detection and distribution of the endosymbiont Wolbachia of Dirofilaria immitis and Brugia pahangi using a polyclonal antiserum raised against WSP (Wolbachia surface protein). Parasitol Res 89(5):381–386. https://doi.org/10.1007/s00436-002-0765-6

    Article  CAS  PubMed  Google Scholar 

  16. Lichtman JW, Conchello JA (2005) Fluorescence microscopy. Nat Methods 2(12):910–919. https://doi.org/10.1038/nmeth817

    Article  CAS  PubMed  Google Scholar 

  17. Sanderson MJ, Smith I, Parker I et al (2014) Fluorescence microscopy. Cold Spring Harb Protoc 2014 (10):pdb.top071795. https://doi.org/10.1101/pdb.top071795

  18. Combs CA (2010) Fluorescence microscopy: a concise guide to current imaging methods. Curr Protoc Neurosci Chapter 2(Unit2):1. https://doi.org/10.1002/0471142301.ns0201s50

    Article  Google Scholar 

  19. White J (2014) Reflecting on confocal microscopy: a personal perspective. Methods Mol Biol 1075:1–7. https://doi.org/10.1007/978-1-60761-847-8_1

    Article  PubMed  Google Scholar 

  20. Paddock SW, Eliceiri KW (2014) Laser scanning confocal microscopy: history, applications, and related optical sectioning techniques. In: Paddock SW (ed) Confocal microscopy methods and protocols, Methods in molecular biology, vol 1075. Humana, New York, pp 9–47

    Chapter  Google Scholar 

  21. Swedlow JR (2013) Quantitative fluorescence microscopy and image deconvolution. Methods Cell Biol 114:407–426. https://doi.org/10.1016/b978-0-12-407761-4.00017-8

    Article  PubMed  Google Scholar 

  22. Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248(4951):73–76. https://doi.org/10.1126/science.2321027

    Article  CAS  PubMed  Google Scholar 

  23. Benninger RKP, Piston DW (2013) Two-photon excitation microscopy for the study of living cells and tissues. Curr Protoc Cell Biol Chapter 4:4.11.11–14.11.24. https://doi.org/10.1002/0471143030.cb0411s59

  24. Hadfield SJ, Axton JM (1999) Germ cells colonized by endosymbiotic bacteria. Nature 402(6761):482. https://doi.org/10.1038/45002

    Article  CAS  PubMed  Google Scholar 

  25. Wegel E, Göhler A, Lagerholm BC et al (2016) Imaging cellular structures in super-resolution with SIM, STED and localisation microscopy: a practical comparison. Sci Rep 6:27290. https://doi.org/10.1038/srep27290

  26. Danson AE, McStea A, Wang L et al (2020) Super-resolution fluorescence microscopy reveals clustering behaviour of. Biology (Basel) 9(10). https://doi.org/10.3390/biology9100344

  27. Morales J, Ehret G, Poschmann G et al (2023) Host-symbiont interactions in Angomonas deanei include the evolution of a host-derived dynamin ring around the endosymbiont division site. Curr Biol 33(1):28–40.e27. https://doi.org/10.1016/j.cub.2022.11.020

    Article  CAS  PubMed  Google Scholar 

  28. Kim D, Curthoys NM, Parent MT et al (2013) Bleed-through correction for rendering and correlation analysis in multi-colour localization microscopy. J Opt 15(9). https://doi.org/10.1088/2040-8978/15/9/094011

  29. Shimomura O (2006) Discovery of green fluorescent protein. Methods Biochem Anal 47:1–13

    PubMed  Google Scholar 

  30. Chalfie M, Tu Y, Euskirchen G, Ward WW et al (1994) Green fluorescent protein as a marker for gene expression. Science 263(5148):802–805. https://doi.org/10.1126/science.8303295

    Article  CAS  PubMed  Google Scholar 

  31. Heim R, Cubitt AB, Tsien RY (1995) Improved green fluorescence. Nature 373(6516):663–664. https://doi.org/10.1038/373663b0

    Article  CAS  PubMed  Google Scholar 

  32. Baird GS, Zacharias DA, Tsien RY (2000) Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci U S A 97(22):11984–11989. https://doi.org/10.1073/pnas.97.22.11984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Gross LA, Baird GS, Hoffman RC et al (2000) The structure of the chromophore within DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci U S A 97(22):11990–11995. https://doi.org/10.1073/pnas.97.22.11990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Heikal AA, Hess ST, Baird GS et al (2000) Molecular spectroscopy and dynamics of intrinsically fluorescent proteins: coral red (dsRed) and yellow (Citrine). Proc Natl Acad Sci U S A 97(22):11996–12001. https://doi.org/10.1073/pnas.97.22.11996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Gramates LS, Agapite J, Attrill H et al (2022) FlyBase: a guided tour of highlighted features. Genetics 220(4). https://doi.org/10.1093/genetics/iyac035

  36. Cherry JM, Hong EL, Amundsen C et al (2012) Saccharomyces genome database: the genomics resource of budding yeast. Nucleic Acids Res 40(Database issue):D700-705. https://doi.org/10.1093/nar/gkr1029

  37. Frydman HM, Li JM, Robson DN et al (2006) Somatic stem cell niche tropism in Wolbachia. Nature 441(7092):509–512. https://doi.org/10.1038/nature04756

    Article  CAS  PubMed  Google Scholar 

  38. Serbus LR, Landmann F, Bray WM et al (2012) A cell-based screen reveals that the albendazole metabolite, albendazole sulfone, targets Wolbachia. PLoS Pathog 8(9):e1002922. https://doi.org/10.1371/journal.ppat.1002922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Flores HA, Bubnell JE, Aquadro CF et al (2015) The Drosophila bag of marbles gene interacts genetically with Wolbachia and shows female-specific effects of divergence. PLoS Genet 11(8):e1005453. https://doi.org/10.1371/journal.pgen.1005453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Landmann F, Orsi GA, Loppin B et al (2009) Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. PLoS Pathog 5(3):e1000343. https://doi.org/10.1371/journal.ppat.1000343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Katsuma S, Hirota K, Matsuda-Imai N et al (2022) A Wolbachia factor for male killing in lepidopteran insects. Nat Commun 13(1):6764. https://doi.org/10.1038/s41467-022-34488-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Mayoral JG, Hussain M, Joubert DA et al (2014) Wolbachia small noncoding RNAs and their role in cross-kingdom communications. Proc Natl Acad Sci U S A 111(52):18721–18726. https://doi.org/10.1073/pnas.1420131112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. LePage DP, Jernigan KK, Bordenstein SR (2014) The relative importance of DNA methylation and Dnmt2-mediated epigenetic regulation on Wolbachia densities and cytoplasmic incompatibility. PeerJ 2:e678. https://doi.org/10.7717/peerj.678

    Article  PubMed  PubMed Central  Google Scholar 

  44. Beckmann JF, Sharma GD, Mendez L et al (2019) The Wolbachia cytoplasmic incompatibility enzyme CidB targets nuclear import and protamine-histone exchange factors. elife 8. https://doi.org/10.7554/eLife.50026

  45. Sheehan KB, Martin M, Lesser CF et al (2016) Identification and Characterization of a Candidate Wolbachia pipientis Type IV Effector That Interacts with the Actin Cytoskeleton. mBio 7(4). https://doi.org/10.1128/mBio.00622-16

  46. Rice DW, Sheehan KB, Newton ILG (2017) Large-scale identification of Wolbachia pipientis effectors. Genome Biol Evol 9(7):1925–1937. https://doi.org/10.1093/gbe/evx139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Mills MK, McCabe LG, Rodrigue EM et al (2023) Wbm0076, a candidate effector protein of the Wolbachia endosymbiont of Brugia malayi, disrupts eukaryotic actin dynamics. PLoS Pathog 19(2):e1010777. https://doi.org/10.1371/journal.ppat.1010777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Ote M, Ueyama M, Yamamoto D (2016) Wolbachia protein TomO targets nanos mRNA and restores germ stem cells in Drosophila sex-lethal mutants. Curr Biol 26(17):2223–2232. https://doi.org/10.1016/j.cub.2016.06.054

    Article  CAS  PubMed  Google Scholar 

  49. Adams KL, Abernathy DG, Willett BC et al (2021) Wolbachia cifB induces cytoplasmic incompatibility in the malaria mosquito vector. Nat Microbiol 6(12):1575–1582. https://doi.org/10.1038/s41564-021-00998-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Terretaz K, Horard B, Weill M et al (2023) Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication. PLoS Pathog 19(3):e1011211. https://doi.org/10.1371/journal.ppat.1011211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Horard B, Terretaz K, Gosselin-Grenet AS et al (2022) Paternal transmission of the Wolbachia CidB toxin underlies cytoplasmic incompatibility. Curr Biol 32(6):1319–1331.e1315. https://doi.org/10.1016/j.cub.2022.01.052

    Article  CAS  PubMed  Google Scholar 

  52. Casper-Lindley C, Kimura S, Saxton DS et al (2011) Rapid fluorescence-based screening for Wolbachia endosymbionts in Drosophila germ line and somatic tissues. Appl Environ Microbiol 77(14):4788–4794. https://doi.org/10.1128/aem.00215-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Venard CM, Crain PR, Dobson SL (2011) SYTO11 staining vs FISH staining: a comparison of two methods to stain Wolbachia pipientis in cell cultures. Lett Appl Microbiol 52(2):168–176. https://doi.org/10.1111/j.1472-765X.2010.02986.x

    Article  PubMed  PubMed Central  Google Scholar 

  54. Christensen S, Camacho M, Sharmin Z et al (2019) Quantitative methods for assessing local and bodywide contributions to Wolbachia titer in maternal germline cells of Drosophila. BMC Microbiol 19(1):206. https://doi.org/10.1186/s12866-019-1579-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Fischer K, Beatty WL, Jiang D et al (2011) Tissue and stage-specific distribution of Wolbachia in Brugia malayi. PLoS Negl Trop Dis 5(5):e1174. https://doi.org/10.1371/journal.pntd.0001174

    Article  PubMed  PubMed Central  Google Scholar 

  56. Inácio da Silva LM, Dezordi FZ, Paiva MHS et al (2021) Systematic review of Wolbachia symbiont detection in mosquitoes: an entangled topic about methodological power and true Symbiosis. Pathogens 10(1). https://doi.org/10.3390/pathogens10010039

  57. O’Neill SL, Karr TL (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348(6297):178–180. https://doi.org/10.1038/348178a0

    Article  PubMed  Google Scholar 

  58. Glover DM, Raff J, Karr TL et al (1990) Parasites in Drosophila embryos. Nature 348(6297):117. https://doi.org/10.1038/348117a0

    Article  CAS  PubMed  Google Scholar 

  59. Callaini G, Riparbelli MG, Dallai R (1994) The distribution of cytoplasmic bacteria in the early Drosophila embryo is mediated by astral microtubules. J Cell Sci 107(Pt 3):673–682. https://doi.org/10.1242/jcs.107.3.673

    Article  PubMed  Google Scholar 

  60. White PM, Serbus LR, Debec A et al (2017) Reliance of Wolbachia on high rates of host proteolysis revealed by a genome-wide RNAi screen of Drosophila cells. Genetics 205(4):1473–1488. https://doi.org/10.1534/genetics.116.198903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Bressac C, Rousset F (1993) The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J Invertebr Pathol 61(3):226–230. https://doi.org/10.1006/jipa.1993.1044

    Article  CAS  PubMed  Google Scholar 

  62. Dedeine F, Vavre F, Fleury F et al (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci U S A 98(11):6247–6252. https://doi.org/10.1073/pnas.101304298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Ferree PM, Frydman HM, Li JM et al (2005) Wolbachia utilizes host microtubules and dynein for anterior localization in the Drosophila oocyte. PLoS Pathog 1(2):e14. https://doi.org/10.1371/journal.ppat.0010014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Landmann F, Foster JM, Slatko B, Sullivan W (2010) Asymmetric Wolbachia segregation during early Brugia malayi embryogenesis determines its distribution in adult host tissues. PLoS Negl Trop Dis 4(7):e758. https://doi.org/10.1371/journal.pntd.0000758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Radousky YA, Hague MTJ, Fowler S et al (2023) Distinct Wolbachia localization patterns in oocytes of diverse host species reveal multiple strategies of maternal transmission. Genetics. https://doi.org/10.1093/genetics/iyad038

  66. Kose H, Karr TL (1995) Organization of Wolbachia pipientis in the drosophila fertilized egg and embryo revealed by an anti-Wolbachia monoclonal antibody. Mech Dev 51(2–3):275–288. https://doi.org/10.1016/0925-4773(95)00372-x

    Article  CAS  PubMed  Google Scholar 

  67. Funkhouser-Jones LJ, van Opstal EJ, Sharma A et al (2018) The maternal effect gene Wds controls Wolbachia Titer in Nasonia. Curr Biol 28(11):1692–1702.e1696. https://doi.org/10.1016/j.cub.2018.04.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Tárnok A (2008) SYTO dyes and histoproteins--myriad of applications. Cytometry A 73 (6):477–479. https://doi.org/10.1002/cyto.a.20588

  69. Albertson R, Casper-Lindley C, Cao J et al (2009) Symmetric and asymmetric mitotic segregation patterns influence Wolbachia distribution in host somatic tissue. J Cell Sci 122(Pt 24):4570–4583. https://doi.org/10.1242/jcs.054981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Clare RH, Cook DA, Johnston KL et al (2015) Development and validation of a high-throughput anti-Wolbachia whole-cell screen: a route to macrofilaricidal drugs against onchocerciasis and lymphatic filariasis. J Biomol Screen 20(1):64–69. https://doi.org/10.1177/1087057114551518

    Article  CAS  PubMed  Google Scholar 

  71. Serbus LR, Ferreccio A, Zhukova M et al (2011) A feedback loop between Wolbachia and the drosophila gurken mRNP complex influences Wolbachia titer. J Cell Sci 124(Pt 24):4299–4308. https://doi.org/10.1242/jcs.092510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Rasgon JL, Gamston CE, Ren X (2006) Survival of Wolbachia pipientis in cell-free medium. Appl Environ Microbiol 72(11):6934–6937. https://doi.org/10.1128/aem.01673-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Nevalainen LB, Layton EM, Newton ILG (2023) Wolbachia promotes its own uptake by host cells. Infect Immun 91(2):e0055722. https://doi.org/10.1128/iai.00557-22

    Article  CAS  PubMed  Google Scholar 

  74. Im K, Mareninov S, Diaz MFP et al (2019) An introduction to performing immunofluorescence staining. Methods Mol Biol 1897:299–311. https://doi.org/10.1007/978-1-4939-8935-5_26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Toomey ME, Panaram K, Fast EM et al (2013) Evolutionarily conserved Wolbachia-encoded factors control pattern of stem-cell niche tropism in drosophila ovaries and favor infection. Proc Natl Acad Sci U S A 110(26):10788–10793. https://doi.org/10.1073/pnas.1301524110

    Article  PubMed  PubMed Central  Google Scholar 

  76. Hargitai D, Kenéz L, Al-Lami M et al (2022) Autophagy controls Wolbachia infection upon bacterial damage and in aging drosophila. Front Cell Dev Biol 10:976882. https://doi.org/10.3389/fcell.2022.976882

    Article  PubMed  PubMed Central  Google Scholar 

  77. Min KT, Benzer S (1997) Wolbachia, normally a symbiont of drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci U S A 94(20):10792–10796. https://doi.org/10.1073/pnas.94.20.10792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Braig HR, Zhou W, Dobson SL et al (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol 180(9):2373–2378. https://doi.org/10.1128/jb.180.9.2373-2378.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Dobson SL, Bourtzis K, Braig HR et al (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem Mol Biol 29(2):153–160. https://doi.org/10.1016/s0965-1748(98)00119-2

    Article  CAS  PubMed  Google Scholar 

  80. Lu P, Bian G, Pan X et al (2012) Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis 6(7):e1754. https://doi.org/10.1371/journal.pntd.0001754

    Article  PubMed  PubMed Central  Google Scholar 

  81. Chevignon G, Foray V, Pérez-Jiménez MM et al (2021) Dual RNAseq analyses at soma and germline levels reveal evolutionary innovations in the elephantiasis-agent Brugia malayi, and adaptation of its Wolbachia endosymbionts. PLoS Negl Trop Dis 15(1):e0008935. https://doi.org/10.1371/journal.pntd.0008935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Turner JD, Langley RS, Johnston KL et al (2009) Wolbachia lipoprotein stimulates innate and adaptive immunity through toll-like receptors 2 and 6 to induce disease manifestations of filariasis. J Biol Chem 284(33):22364–22378. https://doi.org/10.1074/jbc.M901528200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Li Z, Carlow CK (2012) Characterization of transcription factors that regulate the type IV secretion system and riboflavin biosynthesis in Wolbachia of Brugia malayi. PLoS One 7(12):e51597. https://doi.org/10.1371/journal.pone.0051597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Sinha A, Li Z, Sun L, Carlow CKS (2019) Complete genome sequence of the Wolbachia wAlbB endosymbiont of Aedes albopictus. Genome Biol Evol 11(3):706–720. https://doi.org/10.1093/gbe/evz025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. McGraw EA, Merritt DJ, Droller JN et al (2002) Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci U S A 99(5):2918–2923. https://doi.org/10.1073/pnas.052466499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Guo Y, Hoffmann AA, Xu XQ et al (2018) Vertical transmission of Wolbachia is associated with host Vitellogenin transmission in Laodelphax striatellus. Front Microbiol 9:2016. https://doi.org/10.3389/fmicb.2018.02016

    Article  PubMed  PubMed Central  Google Scholar 

  87. McLaughlin JM, Bratu DP (2015) Drosophila melanogaster Oogenesis: An Overview. Methods Mol Biol 1328:1–20. https://doi.org/10.1007/978-1-4939-2851-4_1

    Article  CAS  PubMed  Google Scholar 

  88. Toomey ME, Frydman HM (2014) Extreme divergence of Wolbachia tropism for the stem-cell-niche in the drosophila testis. PLoS Pathog 10(12):e1004577. https://doi.org/10.1371/journal.ppat.1004577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Serbus LR, Sullivan W (2007) A cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog 3(12):e190. https://doi.org/10.1371/journal.ppat.0030190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Landmann F, Bain O, Martin C et al (2012) Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes. Biol Open 1(6):536–547. https://doi.org/10.1242/bio.2012737

    Article  PubMed  PubMed Central  Google Scholar 

  91. Haeusser DP, Margolin W (2016) Splitsville: structural and functional insights into the dynamic bacterial Z ring. Nat Rev Microbiol 14(5):305–319. https://doi.org/10.1038/nrmicro.2016.26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Landmann F, Foster JM, Michalski ML et al (2014) Co-evolution between an endosymbiont and its nematode host: Wolbachia asymmetric posterior localization and AP polarity establishment. PLoS Negl Trop Dis 8(8):e3096. https://doi.org/10.1371/journal.pntd.0003096

    Article  PubMed  PubMed Central  Google Scholar 

  93. Cho KO (2004) Wolbachia bacteria, the cause for false vesicular staining pattern in Drosophila melanogaster. Gene Expr Patterns 5(2):167–170. https://doi.org/10.1016/j.modgep.2004.08.008

    Article  CAS  PubMed  Google Scholar 

  94. Albertson R, Tan V, Leads RR et al (2013) Mapping Wolbachia distributions in the adult drosophila brain. Cell Microbiol 15(9):1527–1544. https://doi.org/10.1111/cmi.12136

    Article  CAS  PubMed  Google Scholar 

  95. Beckmann JF, Ronau JA, Hochstrasser M (2017) A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat Microbiol 2:17007. https://doi.org/10.1038/nmicrobiol.2017.7

    Article  PubMed  PubMed Central  Google Scholar 

  96. Voronin D, Cook DA, Steven A et al (2012) Autophagy regulates Wolbachia populations across diverse symbiotic associations. Proc Natl Acad Sci U S A 109(25):E1638–E1646. https://doi.org/10.1073/pnas.1203519109

    Article  PubMed  PubMed Central  Google Scholar 

  97. Strunov A, Schmidt K, Kapun M et al (2022) Restriction of Wolbachia bacteria in early embryogenesis of Neotropical drosophila species via endoplasmic reticulum-mediated autophagy. MBio 13(2):e0386321. https://doi.org/10.1128/mbio.03863-21

    Article  CAS  PubMed  Google Scholar 

  98. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6(10):741–751. https://doi.org/10.1038/nrmicro1969

    Article  CAS  PubMed  Google Scholar 

  99. Serbus LR, Casper-Lindley C, Landmann F, Sullivan W (2008) The genetics and cell biology of Wolbachia-host interactions. Annu Rev Genet 42:683–707. https://doi.org/10.1146/annurev.genet.41.110306.130354

    Article  CAS  PubMed  Google Scholar 

  100. Lassy CW, Karr TL (1996) Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans. Mech Dev 57(1):47–58. https://doi.org/10.1016/0925-4773(96)00527-8

    Article  CAS  PubMed  Google Scholar 

  101. Bonneau M, Landmann F, Labbé P, Justy F, Weill M, Sicard M (2018) The cellular phenotype of cytoplasmic incompatibility in Culex pipiens in the light of cidB diversity. PLoS Pathog 14(10):e1007364. https://doi.org/10.1371/journal.ppat.1007364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Riparbelli MG, Giordano R, Ueyama M et al (2012) Wolbachia-mediated male killing is associated with defective chromatin remodeling. PLoS One 7(1):e30045. https://doi.org/10.1371/journal.pone.0030045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Harumoto T, Fukatsu T (1875) Lemaitre B (2018) common and unique strategies of male killing evolved in two distinct drosophila symbionts. Proc Biol Sci 285. https://doi.org/10.1098/rspb.2017.2167

  104. Teixeira L, Ferreira A, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6(12):e2. https://doi.org/10.1371/journal.pbio.1000002

    Article  CAS  PubMed  Google Scholar 

  105. Hedges LM, Brownlie JC, O’Neill SL et al (2008) Wolbachia and virus protection in insects. Science 322(5902):702. https://doi.org/10.1126/science.1162418

    Article  CAS  PubMed  Google Scholar 

  106. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA et al (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and plasmodium. Cell 139(7):1268–1278. https://doi.org/10.1016/j.cell.2009.11.042

    Article  PubMed  Google Scholar 

  107. Altinli M, Soms J, Ravallec M et al (2018) Sharing cells with Wolbachia: the transovarian vertical transmission of Culex pipiens densovirus. Environ Microbiol. https://doi.org/10.1111/1462-2920.14511

  108. Bishop R (2010) Applications of fluorescence in situ hybridization (FISH) in detecting genetic aberrations of medical significance. Bioscience Horizons 3(1):85–95. https://doi.org/10.1093/biohorizons/hzq009

    Article  CAS  Google Scholar 

  109. Cha BJ, Serbus LR, Koppetsch BS et al (2002) Kinesin I-dependent cortical exclusion restricts pole plasm to the oocyte posterior. Nat Cell Biol 4(8):592–598. https://doi.org/10.1038/ncb832

    Article  CAS  PubMed  Google Scholar 

  110. Strunov A, Schneider DI, Albertson R et al (2017) Restricted distribution and lateralization of mutualistic Wolbachia in the drosophila brain. Cell Microbiol 19(1). https://doi.org/10.1111/cmi.12639

  111. Newton IL, Savytskyy O, Sheehan KB (2015) Wolbachia utilize host actin for efficient maternal transmission in Drosophila melanogaster. PLoS Pathog 11(4):e1004798. https://doi.org/10.1371/journal.ppat.1004798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Heddi A, Grenier AM, Khatchadourian C et al (1999) Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc Natl Acad Sci U S A 96(12):6814–6819. https://doi.org/10.1073/pnas.96.12.6814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Dodson BL, Hughes GL, Paul O et al (2014) Wolbachia enhances West Nile virus (WNV) infection in the mosquito Culex tarsalis. PLoS Negl Trop Dis 8(7):e2965. https://doi.org/10.1371/journal.pntd.0002965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Gong JT, Li Y, Li TP et al (2020) Stable introduction of plant-virus-inhibiting Wolbachia into Planthoppers for Rice protection. Curr Biol 30(24):4837–4845.e4835. https://doi.org/10.1016/j.cub.2020.09.033

    Article  CAS  PubMed  Google Scholar 

  115. Hughes GL, Pike AD, Xue P et al (2012) Invasion of Wolbachia into anopheles and other insect germlines in an ex vivo organ culture system. PLoS One 7(4):e36277. https://doi.org/10.1371/journal.pone.0036277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Uribe-Alvarez C, Chiquete-Felix N, Morales-Garcia L et al (2019) Wolbachia pipientis grows in Saccharomyces cerevisiae evoking early death of the host and deregulation of mitochondrial metabolism. Microbiology 8(4):e00675. https://doi.org/10.1002/mbo3.675

    Article  CAS  Google Scholar 

  117. Brown AM, Wasala SK, Howe DK et al (2016) Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts. Sci Rep 6:34955. https://doi.org/10.1038/srep34955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Deehan M, Lin W, Blum B et al (2021) Intracellular density of Wolbachia is mediated by host autophagy and the bacterial cytoplasmic incompatibility gene cifB in a cell type-dependent manner in Drosophila melanogaster. mBio 12(1). https://doi.org/10.1128/mBio.02205-20

  119. Kamath AD, Deehan MA, Frydman HM (2018) Polar cell fate stimulates Wolbachia intracellular growth. Development 145(6). https://doi.org/10.1242/dev.158097

  120. Strunov A, Kiseleva E, Gottlieb Y (2013) Spatial and temporal distribution of pathogenic Wolbachia strain wMelPop in Drosophila melanogaster central nervous system under different temperature conditions. J Invertebr Pathol 114(1):22–30. https://doi.org/10.1016/j.jip.2013.05.001

    Article  PubMed  Google Scholar 

  121. Genty LM, Bouchon D, Raimond M et al (2014) Wolbachia infect ovaries in the course of their maturation: last minute passengers and priority travellers? PLoS One 9(4):e94577. https://doi.org/10.1371/journal.pone.0094577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Khoo CC, Venard CM, Fu Y et al (2013) Infection, growth and maintenance of Wolbachia pipientis in clonal and non-clonal Aedes albopictus cell cultures. Bull Entomol Res 103(3):251–260. https://doi.org/10.1017/s0007485312000648

    Article  CAS  PubMed  Google Scholar 

  123. Grobler Y, Yun CY, Kahler DJ et al (2018) Whole genome screen reveals a novel relationship between Wolbachia levels and drosophila host translation. PLoS Pathog 14(11):e1007445. https://doi.org/10.1371/journal.ppat.1007445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Xi Z, Dobson SL (2005) Characterization of Wolbachia transfection efficiency by using microinjection of embryonic cytoplasm and embryo homogenate. Appl Environ Microbiol 71(6):3199–3204. https://doi.org/10.1128/aem.71.6.3199-3204.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Gottlieb Y, Ghanim M, Gueguen G et al (2008) Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J 22(7):2591–2599. https://doi.org/10.1096/fj.07-101162

    Article  CAS  PubMed  Google Scholar 

  126. Hosokawa T, Koga R, Kikuchi Y et al (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci U S A 107(2):769–774. https://doi.org/10.1073/pnas.0911476107

    Article  PubMed  Google Scholar 

  127. Schneider DI, Parker AG, Abd-Alla AM et al (2018) High-sensitivity detection of cryptic Wolbachia in the African tsetse fly (Glossina spp.). BMC Microbiol 18(Suppl 1):140. https://doi.org/10.1186/s12866-018-1291-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Bian G, Joshi D, Dong Y et al (2013) Wolbachia invades Anopheles stephensi populations and induces refractoriness to plasmodium infection. Science 340(6133):748–751. https://doi.org/10.1126/science.1236192

    Article  CAS  PubMed  Google Scholar 

  129. Kaur R, Martinez J, Rota-Stabelli O et al (2020) Age, tissue, genotype and virus infection regulate Wolbachia levels in drosophila. Mol Ecol 29(11):2063–2079. https://doi.org/10.1111/mec.15462

    Article  CAS  PubMed  Google Scholar 

  130. Hughes GL, Koga R, Xue P et al (2011) Wolbachia infections are virulent and inhibit the human malaria parasite plasmodium falciparum in Anopheles gambiae. PLoS Pathog 7(5):e1002043. https://doi.org/10.1371/journal.ppat.1002043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Blawid R, Morgado FS, Souza CA et al (2015) Fluorescence in situ hybridization analysis of endosymbiont genera reveals novel infection patterns in a tomato-infesting Bemisia tabaci population from Brazil. Trop Plant Pathol 40:233–243

    Article  Google Scholar 

  132. Ren SL, Li YH, Ou D et al (2018) Localization and dynamics of Wolbachia infection in Asian citrus psyllid Diaphorina citri, the insect vector of the causal pathogens of Huanglongbing. Microbiology 7(3):e00561. https://doi.org/10.1002/mbo3.561

    Article  Google Scholar 

  133. Wangkeeree J, Tewaruxsa P, Roddee J et al (2020) Wolbachia (Rickettsiales: Alphaproteobacteria) infection in the leafhopper vector of sugarcane White leaf disease. J Insect Sci 20:3. https://doi.org/10.1093/jisesa/ieaa053

    Article  Google Scholar 

  134. Ant TH, Herd CS, Geoghegan V et al (2018) The Wolbachia strain wAu provides highly efficient virus transmission blocking in Aedes aegypti. PLoS Pathog 14(1):e1006815. https://doi.org/10.1371/journal.ppat.1006815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Dunning Hotopp JC, Clark ME, Oliveira DC et al (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317(5845):1753–1756. https://doi.org/10.1126/science.1142490

    Article  CAS  PubMed  Google Scholar 

  136. Klasson L, Kumar N, Bromley R et al (2014) Extensive duplication of the Wolbachia DNA in chromosome four of Drosophila ananassae. BMC Genomics 15(1):1097. https://doi.org/10.1186/1471-2164-15-1097

    Article  PubMed  PubMed Central  Google Scholar 

  137. Tvedte ES, Gasser M, Zhao X et al (2022) Accumulation of endosymbiont genomes in an insect autosome followed by endosymbiont replacement. Curr Biol 32(12):2786–2795.e2785. https://doi.org/10.1016/j.cub.2022.05.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Nikoh N, Tanaka K, Shibata F et al (2008) Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 18(2):272–280. https://doi.org/10.1101/gr.7144908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Aikawa T, Anbutsu H, Nikoh N et al (2009) Longicorn beetle that vectors pinewood nematode carries many Wolbachia genes on an autosome. Proc Biol Sci 276(1674):3791–3798. https://doi.org/10.1098/rspb.2009.1022

    Article  PubMed  PubMed Central  Google Scholar 

  140. Funkhouser-Jones LJ, Sehnert SR, Martínez-Rodríguez P et al (2015) Wolbachia co-infection in a hybrid zone: discovery of horizontal gene transfers from two Wolbachia supergroups into an animal genome. PeerJ 3:e1479. https://doi.org/10.7717/peerj.1479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Brelsfoard C, Tsiamis G, Falchetto M et al (2014) Presence of extensive Wolbachia symbiont insertions discovered in the genome of its host Glossina morsitans. PLoS Negl Trop Dis 8(4):e2728. https://doi.org/10.1371/journal.pntd.0002728

    Article  PubMed  PubMed Central  Google Scholar 

  142. Warecki B, Titen SWA, Alam MS et al (2022) Action in the sperm produces developmentally deferred chromosome segregation defects during the. elife 11. https://doi.org/10.7554/eLife.81292

  143. Greenspan P, Mayer EP, Fowler SD (1985) Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100(3):965–973. https://doi.org/10.1083/jcb.100.3.965

    Article  CAS  PubMed  Google Scholar 

  144. Yen K, Le TT, Bansal A, Narasimhan SD et al (2010) A comparative study of fat storage quantitation in nematode Caenorhabditis elegans using label and label-free methods. PLoS One 5(9). https://doi.org/10.1371/journal.pone.0012810

  145. Geoghegan V, Stainton K, Rainey S et al (2017) Perturbed cholesterol and vesicular trafficking associated with dengue blocking in Wolbachia-infected Aedes aegypti cells. Nat Commun 8(1):526. https://doi.org/10.1038/s41467-017-00610-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Conceição CC, da Silva JN, Arcanjo A, Nogueira CL et al (2021) Aedes fluviatilis cell lines as new tools to study metabolic and immune interactions in mosquito-Wolbachia symbiosis. Sci Rep 11(1):19202. https://doi.org/10.1038/s41598-021-98738-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Wang J, Guo X, Li L et al (2018) Application of the fluorescent dye BODIPY in the study of lipid dynamics of the Rice blast fungus. Molecules 23(7). https://doi.org/10.3390/molecules23071594

  148. Rumin J, Bonnefond H, Saint-Jean B et al (2015) The use of fluorescent Nile red and BODIPY for lipid measurement in microalgae. Biotechnol Biofuels 8:42. https://doi.org/10.1186/s13068-015-0220-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Schultz MJ, Tan AL, Gray CN et al (2018) Stri blocks Zika virus growth at two independent stages of viral replication. mBio 9(3). https://doi.org/10.1128/mBio.00738-18

  150. McDonald L, Liu B, Taraboletti A et al (2016) Fluorescent flavonoids for endoplasmic reticulum cell imaging. J Mater Chem B 4(48):7902–7908. https://doi.org/10.1039/c6tb02456d

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Fattouh N, Cazevieille C, Landmann F (2019) Wolbachia endosymbionts subvert the endoplasmic reticulum to acquire host membranes without triggering ER stress. PLoS Negl Trop Dis 13(3):e0007218. https://doi.org/10.1371/journal.pntd.0007218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Tóth B, Balla A, Ma H et al (2006) Phosphatidylinositol 4-kinase IIIbeta regulates the transport of ceramide between the endoplasmic reticulum and Golgi. J Biol Chem 281(47):36369–36377. https://doi.org/10.1074/jbc.M604935200

    Article  CAS  PubMed  Google Scholar 

  153. Kholmukhamedov A, Schwartz JM, Lemasters JJ (2013) Isolated mitochondria infusion mitigates ischemia-reperfusion injury of the liver in rats: mitotracker probes and mitochondrial membrane potential. Shock 39(6):543. https://doi.org/10.1097/SHK.0b013e318292300d

    Article  PubMed  PubMed Central  Google Scholar 

  154. Stowers RS, Megeath LJ, Górska-Andrzejak J et al (2002) Axonal transport of mitochondria to synapses depends on Milton, a novel drosophila protein. Neuron 36(6):1063–1077. https://doi.org/10.1016/s0896-6273(02)01094-2

    Article  CAS  PubMed  Google Scholar 

  155. Russell SL, Lemseffer N, White PM et al (2018) Wolbachia and host germline components compete for kinesin-mediated transport to the posterior pole of the drosophila oocyte. PLoS Pathog 14(8):e1007216. https://doi.org/10.1371/journal.ppat.1007216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Tram U, Sullivan W (2002) Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296(5570):1124–1126. https://doi.org/10.1126/science.1070536

    Article  CAS  PubMed  Google Scholar 

  157. Li L, Wan T, Wan M et al (2015) The effect of the size of fluorescent dextran on its endocytic pathway. Cell Biol Int 39(5):531–539

    Article  CAS  PubMed  Google Scholar 

  158. Larsen BD, Sørensen CS (2017) The caspase-activated DNase: apoptosis and beyond. FEBS J 284(8):1160–1170. https://doi.org/10.1111/febs.13970

    Article  CAS  PubMed  Google Scholar 

  159. Darzynkiewicz Z, Zhao H (2011) Detection of DNA strand breaks in apoptotic cells by flow- and image-cytometry. Methods Mol Biol 682:91–101. https://doi.org/10.1007/978-1-60327-409-8_8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Harumoto T, Anbutsu H, Lemaitre B et al (2016) Male-killing symbiont damages host’s dosage-compensated sex chromosome to induce embryonic apoptosis. Nat Commun 7:12781. https://doi.org/10.1038/ncomms12781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Zhukova MV, Kiseleva E (2012) The virulent Wolbachia strain wMelPop increases the frequency of apoptosis in the female germline cells of Drosophila melanogaster. BMC Microbiol 12 Suppl 1 (Suppl 1):S15. https://doi.org/10.1186/1471-2180-12-s1-s15

  162. Guo Y, Hoffmann AA, Xu XQ et al (2018) Wolbachia-induced apoptosis associated with increased fecundity in Laodelphax striatellus (Hemiptera: Delphacidae). Insect Mol Biol 27(6):796–807. https://doi.org/10.1111/imb.12518

    Article  CAS  PubMed  Google Scholar 

  163. Fast EM, Toomey ME, Panaram K et al (2011) Wolbachia enhance drosophila stem cell proliferation and target the germline stem cell niche. Science 334(6058):990–992. https://doi.org/10.1126/science.1209609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Landmann F, Voronin D, Sullivan W et al (2011) Anti-filarial activity of antibiotic therapy is due to extensive apoptosis after Wolbachia depletion from filarial nematodes. PLoS Pathog 7(11):e1002351. https://doi.org/10.1371/journal.ppat.1002351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Pannebakker BA, Loppin B, Elemans CP et al (2007) Parasitic inhibition of cell death facilitates symbiosis. Proc Natl Acad Sci U S A 104(1):213–215. https://doi.org/10.1073/pnas.0607845104

    Article  CAS  PubMed  Google Scholar 

  166. Kremer N, Voronin D, Charif D et al (2009) Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog 5(10):e1000630. https://doi.org/10.1371/journal.ppat.1000630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Bazzocchi C, Comazzi S, Santoni R et al (2007) Wolbachia surface protein (WSP) inhibits apoptosis in human neutrophils. Parasite Immunol 29(2):73–79. https://doi.org/10.1111/j.1365-3024.2006.00915.x

    Article  CAS  PubMed  Google Scholar 

  168. Voronin D, Bachu S, Shlossman M et al (2016) Glucose and glycogen metabolism in Brugia malayi is associated with Wolbachia symbiont fitness. PLoS One 11(4):e0153812. https://doi.org/10.1371/journal.pone.0153812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Wulf E, Deboben A, Bautz FA et al (1979) Fluorescent phallotoxin, a tool for the visualization of cellular actin. Proc Natl Acad Sci U S A 76(9):4498–4502. https://doi.org/10.1073/pnas.76.9.4498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Vandekerckhove J, Deboben A, Nassal M et al (1985) The phalloidin binding site of F-actin. EMBO J 4(11):2815–2818. https://doi.org/10.1002/j.1460-2075.1985.tb04008.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Riparbelli MG, Giordano R, Callaini G (2007) Effects of Wolbachia on sperm maturation and architecture in Drosophila simulans Riverside. Mech Dev 124(9–10):699–714. https://doi.org/10.1016/j.mod.2007.07.001

    Article  CAS  PubMed  Google Scholar 

  172. Tyler JJ, Allwood EG, Ayscough KR (2016) WASP family proteins, more than Arp2/3 activators. Biochem Soc Trans 44(5):1339–1345. https://doi.org/10.1042/bst20160176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Taupin P (2007) BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev 53(1):198–214. https://doi.org/10.1016/j.brainresrev.2006.08.002

    Article  CAS  PubMed  Google Scholar 

  174. Fallon AM, Witthuhn BA (2009) Proteasome activity in a naïve mosquito cell line infected with Wolbachia pipientis wAlbB. In Vitro Cell Dev Biol Anim 45(8):460–466. https://doi.org/10.1007/s11626-009-9193-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Ligasová A, Konečný P, Frydrych I et al (2017) Looking for ugly ducklings: the role of the stability of BrdU-antibody complex and the improved method of the detection of DNA replication. PLoS One 12(3):e0174893. https://doi.org/10.1371/journal.pone.0174893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Cappella P, Gasparri F, Pulici M et al (2008) A novel method based on click chemistry, which overcomes limitations of cell cycle analysis by classical determination of BrdU incorporation, allowing multiplex antibody staining. Cytometry A 73(7):626–636. https://doi.org/10.1002/cyto.a.20582

    Article  CAS  PubMed  Google Scholar 

  177. Foray V, Pérez-Jiménez MM, Fattouh N et al (2018) Wolbachia control stem cell behavior and stimulate germline proliferation in filarial nematodes. Dev Cell 45(2):198–211.e193. https://doi.org/10.1016/j.devcel.2018.03.017

Download references

Acknowledgments

This chapter emphasized primary sources for field-specific fluorescence methods and the diversity of systems applying these methods, with highlights featured to the maximum extent possible. Due to the number of fluorescence-inclusive Wolbachia publications, this chapter was not able to reference every single one. I sincerely apologize to authors whose works were not cited. I am deeply grateful to the hundreds of researchers whose hard work made this review possible. Thanks also to Dr. Fallon for managing this submission, Laura Ochoa for proofreading this manuscript, and the Department of Biological Sciences at Florida International University for their support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laura Renee Serbus .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2024 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Serbus, L.R. (2024). A Light in the Dark: Uncovering Wolbachia-Host Interactions Using Fluorescence Imaging. In: Fallon, A.M. (eds) Wolbachia. Methods in Molecular Biology, vol 2739. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3553-7_21

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-3553-7_21

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-3552-0

  • Online ISBN: 978-1-0716-3553-7

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics