Literature DB >> 23744038

Evolutionarily conserved Wolbachia-encoded factors control pattern of stem-cell niche tropism in Drosophila ovaries and favor infection.

Michelle E Toomey1, Kanchana Panaram, Eva M Fast, Catherine Beatty, Horacio M Frydman.   

Abstract

Wolbachia are intracellular bacteria that infect invertebrates at pandemic levels, including insect vectors of devastating infectious diseases. Although Wolbachia are providing novel strategies for the control of several human pathogens, the processes underlying Wolbachia's successful propagation within and across species remain elusive. Wolbachia are mainly vertically transmitted; however, there is also evidence of extensive horizontal transmission. Here, we provide several lines of evidence supporting Wolbachia's targeting of ovarian stem cell niches--referred to as "niche tropism"--as a previously overlooked strategy for Wolbachia thriving in nature. Niche tropism is pervasive in Wolbachia infecting the Drosophila genus, and different patterns of niche tropism are evolutionarily conserved. Phylogenetic analysis, confirmed by hybrid introgression and transinfection experiments, demonstrates that bacterial factors are the major determinants of differential patterns of niche tropism. Furthermore, bacterial load is increased in germ-line cells passing through infected niches, supporting previous suggestions of a contribution of Wolbachia from stem-cell niches toward vertical transmission. These results support the role of stem-cell niches as a key component for the spreading of Wolbachia in the Drosophila genus and provide mechanistic insights into this unique tissue tropism.

Entities:  

Keywords:  endosymbiont; germline stem cell niche; maternal transmission; microbial tissue tropism; somatic stem cell niche

Mesh:

Substances:

Year:  2013        PMID: 23744038      PMCID: PMC3696799          DOI: 10.1073/pnas.1301524110

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  39 in total

1.  Germ cells colonized by endosymbiotic bacteria.

Authors:  S J Hadfield; J M Axton
Journal:  Nature       Date:  1999-12-02       Impact factor: 49.962

2.  Somatic stem cell niche tropism in Wolbachia.

Authors:  Horacio M Frydman; Jennifer M Li; Drew N Robson; Eric Wieschaus
Journal:  Nature       Date:  2006-05-25       Impact factor: 49.962

3.  Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission.

Authors:  A A Hoffmann; B L Montgomery; J Popovici; I Iturbe-Ormaetxe; P H Johnson; F Muzzi; M Greenfield; M Durkan; Y S Leong; Y Dong; H Cook; J Axford; A G Callahan; N Kenny; C Omodei; E A McGraw; P A Ryan; S A Ritchie; M Turelli; S L O'Neill
Journal:  Nature       Date:  2011-08-24       Impact factor: 49.962

4.  The follicle cells are a major site of vitellogenin synthesis in Drosophila melanogaster.

Authors:  M D Brennan; A J Weiner; T J Goralski; A P Mahowald
Journal:  Dev Biol       Date:  1982-01       Impact factor: 3.582

5.  Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche.

Authors:  Eva M Fast; Michelle E Toomey; Kanchana Panaram; Danielle Desjardins; Eric D Kolaczyk; Horacio M Frydman
Journal:  Science       Date:  2011-10-20       Impact factor: 47.728

6.  Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp.

Authors:  Q Cheng; T D Ruel; W Zhou; S K Moloo; P Majiwa; S L O'Neill; S Aksoy
Journal:  Med Vet Entomol       Date:  2000-03       Impact factor: 2.739

7.  Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg.

Authors:  K Illmensee; A P Mahowald
Journal:  Proc Natl Acad Sci U S A       Date:  1974-04       Impact factor: 11.205

8.  Asymmetric Wolbachia segregation during early Brugia malayi embryogenesis determines its distribution in adult host tissues.

Authors:  Frédéric Landmann; Jeremy M Foster; Barton Slatko; William Sullivan
Journal:  PLoS Negl Trop Dis       Date:  2010-07-27

9.  Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis.

Authors:  D Drummond-Barbosa; A C Spradling
Journal:  Dev Biol       Date:  2001-03-01       Impact factor: 3.582

10.  The diversity and evolution of Wolbachia ankyrin repeat domain genes.

Authors:  Stefanos Siozios; Panagiotis Ioannidis; Lisa Klasson; Siv G E Andersson; Henk R Braig; Kostas Bourtzis
Journal:  PLoS One       Date:  2013-02-04       Impact factor: 3.240

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  40 in total

1.  Mechanisms of Horizontal Cell-to-Cell Transfer of Wolbachia spp. in Drosophila melanogaster.

Authors:  Pamela M White; Jose E Pietri; Alain Debec; Shelbi Russell; Bhavin Patel; William Sullivan
Journal:  Appl Environ Microbiol       Date:  2017-03-17       Impact factor: 4.792

Review 2.  Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses.

Authors:  Alex C C Wilson; Rebecca P Duncan
Journal:  Proc Natl Acad Sci U S A       Date:  2015-05-26       Impact factor: 11.205

3.  Variable Inhibition of Zika Virus Replication by Different Wolbachia Strains in Mosquito Cell Cultures.

Authors:  Michaela J Schultz; Sharon Isern; Scott F Michael; Ronald B Corley; John H Connor; Horacio M Frydman
Journal:  J Virol       Date:  2017-06-26       Impact factor: 5.103

4.  The Drosophila bag of marbles Gene Interacts Genetically with Wolbachia and Shows Female-Specific Effects of Divergence.

Authors:  Heather A Flores; Jaclyn E Bubnell; Charles F Aquadro; Daniel A Barbash
Journal:  PLoS Genet       Date:  2015-08-20       Impact factor: 5.917

5.  Chromosomal localization of Wolbachia inserts in the genomes of two subspecies of Chorthippus parallelus forming a Pyrenean hybrid zone.

Authors:  Raquel Toribio-Fernández; José L Bella; Paloma Martínez-Rodríguez; Lisa J Funkhouser-Jones; Seth R Bordenstein; Miguel Pita
Journal:  Chromosome Res       Date:  2017-05-05       Impact factor: 5.239

6.  Polar cell fate stimulates Wolbachia intracellular growth.

Authors:  Ajit D Kamath; Mark A Deehan; Horacio M Frydman
Journal:  Development       Date:  2018-03-23       Impact factor: 6.868

Review 7.  Local and Physiological Control of Germline Stem Cell Lineages in Drosophila melanogaster.

Authors:  Daniela Drummond-Barbosa
Journal:  Genetics       Date:  2019-09       Impact factor: 4.562

8.  Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes.

Authors:  Grant L Hughes; Brittany L Dodson; Rebecca M Johnson; Courtney C Murdock; Hitoshi Tsujimoto; Yasutsugu Suzuki; Alyssa A Patt; Long Cui; Carlos W Nossa; Rhiannon M Barry; Joyce M Sakamoto; Emily A Hornett; Jason L Rasgon
Journal:  Proc Natl Acad Sci U S A       Date:  2014-08-11       Impact factor: 11.205

9.  Transovarian Transmission of Blochmannia and Wolbachia Endosymbionts in the Neotropical Weaver Ant Camponotus textor (Hymenoptera, Formicidae).

Authors:  Manuela Oliveira Ramalho; Alexsandro Santana Vieira; Mayara Cristina Pereira; Corrie Saux Moreau; Odair Correa Bueno
Journal:  Curr Microbiol       Date:  2018-02-21       Impact factor: 2.188

Review 10.  Evolutionary Ecology of Wolbachia Releases for Disease Control.

Authors:  Perran A Ross; Michael Turelli; Ary A Hoffmann
Journal:  Annu Rev Genet       Date:  2019-09-10       Impact factor: 16.830

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