The chlamydial organism Simkania negevensis forms ER vacuole contact sites and inhibits ER-stress

Adrian Mehlitz, Karthika Karunakaran, Jo-Ana Herweg, Georg Krohne, Sebastian van de Linde, Elke Rieck, Markus Sauer, Thomas Rudel

Research output: Contribution to journalArticle

29 Citations (Scopus)

Abstract

Most intracellular bacterial pathogens reside within membrane-surrounded host-derived vacuoles. Few of these bacteria exploit membranes from the host's endoplasmic reticulum (ER) to form a replicative vacuole. Here, we describe the formation of ER-vacuole contact sites as part of the replicative niche of the chlamydial organism Simkania negevensis. Formation of ER-vacuole contact sites is evolutionary conserved in the distantly related protozoan host Acanthamoeba castellanii. Simkania growth is accompanied by mitochondria associating with the Simkania-containing vacuole (SCV). Super-resolution microscopy as well as 3D reconstruction from electron micrographs of serial ultra-thin sections revealed a single vacuolar system forming extensive ER-SCV contact sites on the Simkania vacuolar surface. Simkania infection induced an ER-stress response, which was later downregulated. Induction of ER-stress with Thapsigargin or Tunicamycin was strongly inhibited in cells infected with Simkania. Inhibition of ER-stress was required for inclusion formation and efficient growth, demonstrating a role of ER-stress in the control of Simkania infection. Thus, Simkania forms extensive ER-SCV contact sites in host species evolutionary as diverse as human and amoeba. Moreover, Simkania is the first bacterial pathogen described to interfere with ER-stress induced signalling to promote infection.

LanguageEnglish
Pages1224-1243
Number of pages20
JournalCellular Microbiology
Volume16
Issue number8
Early online date21 Mar 2014
DOIs
Publication statusPublished - 26 Jul 2014
Externally publishedYes

Fingerprint

Endoplasmic Reticulum Stress
Vacuoles
Endoplasmic Reticulum
Acanthamoeba castellanii
Tunicamycin
Amoeba
Thapsigargin
Membranes
Infection Control
Growth
Infection
Microscopy
Mitochondria
Down-Regulation
Electrons
Bacteria

Keywords

  • vacuoles
  • endoplasmic reticulum
  • ER–vacuole contact
  • super-resolution microscopy
  • electron micrographs
  • Thapsigargin
  • Tunicamycin
  • ER-stress
  • Simkania negevensis
  • Chlamydia

Cite this

Mehlitz, Adrian ; Karunakaran, Karthika ; Herweg, Jo-Ana ; Krohne, Georg ; van de Linde, Sebastian ; Rieck, Elke ; Sauer, Markus ; Rudel, Thomas. / The chlamydial organism Simkania negevensis forms ER vacuole contact sites and inhibits ER-stress. In: Cellular Microbiology. 2014 ; Vol. 16, No. 8. pp. 1224-1243.
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Mehlitz, A, Karunakaran, K, Herweg, J-A, Krohne, G, van de Linde, S, Rieck, E, Sauer, M & Rudel, T 2014, 'The chlamydial organism Simkania negevensis forms ER vacuole contact sites and inhibits ER-stress' Cellular Microbiology, vol. 16, no. 8, pp. 1224-1243. https://doi.org/10.1111/cmi.12278

The chlamydial organism Simkania negevensis forms ER vacuole contact sites and inhibits ER-stress. / Mehlitz, Adrian; Karunakaran, Karthika; Herweg, Jo-Ana; Krohne, Georg; van de Linde, Sebastian; Rieck, Elke; Sauer, Markus; Rudel, Thomas.

In: Cellular Microbiology, Vol. 16, No. 8, 26.07.2014, p. 1224-1243.

Research output: Contribution to journalArticle

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T1 - The chlamydial organism Simkania negevensis forms ER vacuole contact sites and inhibits ER-stress

AU - Mehlitz, Adrian

AU - Karunakaran, Karthika

AU - Herweg, Jo-Ana

AU - Krohne, Georg

AU - van de Linde, Sebastian

AU - Rieck, Elke

AU - Sauer, Markus

AU - Rudel, Thomas

N1 - © 2014 John Wiley & Sons Ltd.

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Y1 - 2014/7/26

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AB - Most intracellular bacterial pathogens reside within membrane-surrounded host-derived vacuoles. Few of these bacteria exploit membranes from the host's endoplasmic reticulum (ER) to form a replicative vacuole. Here, we describe the formation of ER-vacuole contact sites as part of the replicative niche of the chlamydial organism Simkania negevensis. Formation of ER-vacuole contact sites is evolutionary conserved in the distantly related protozoan host Acanthamoeba castellanii. Simkania growth is accompanied by mitochondria associating with the Simkania-containing vacuole (SCV). Super-resolution microscopy as well as 3D reconstruction from electron micrographs of serial ultra-thin sections revealed a single vacuolar system forming extensive ER-SCV contact sites on the Simkania vacuolar surface. Simkania infection induced an ER-stress response, which was later downregulated. Induction of ER-stress with Thapsigargin or Tunicamycin was strongly inhibited in cells infected with Simkania. Inhibition of ER-stress was required for inclusion formation and efficient growth, demonstrating a role of ER-stress in the control of Simkania infection. Thus, Simkania forms extensive ER-SCV contact sites in host species evolutionary as diverse as human and amoeba. Moreover, Simkania is the first bacterial pathogen described to interfere with ER-stress induced signalling to promote infection.

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KW - endoplasmic reticulum

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KW - super-resolution microscopy

KW - electron micrographs

KW - Thapsigargin

KW - Tunicamycin

KW - ER-stress

KW - Simkania negevensis

KW - Chlamydia

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