In vitro reconstitution of Salmonella phagosome-endosome fusion 


 

Principal Investigator : Amitabha Mukhopadhyay

Research Associates/Assistants
Nimisha Sharma
Tapen Dam
Ganga Krishnamurthy

Ph D Students
Konark Mukherjee (till Aug 2000)
Sudha Bala Singh
S Parashuraman
S Senthil Kumar

Pathogenesis of typhoid fever is related to the survival of Salmonella sp. in macrophages. The main goal of this project is to understand the mechanism of survival of Salmonella in macrophages in the pathogenesis. Phagocytosis is an important process in host defense and is mediated by complex interactions between defined intracellular compartments. The final fate of the nascent phagosomes usually culminates with the fusion of lysosomes. But some invading microorganisms modulate this central process for their survival in the phagocytic cells. The major objectives of the present investigations are i) reconstitution of in vitro fusion of Salmonella-containing phagosomes with early endosome to understand the interaction between these two compartments, ii) modulation of Salmonella phagosome and endosome fusion by GTP binding proteins and iii) determination of the role of various signal transduction intermediates in the phagosome endosome fusion.

We have investigated the intracellular route of Salmonella in macrophages to determine a plausible mechanism for their survival in phagocytes. Western blot analysis of isolated phagosomes at different times of their maturation, using specific antibodies revealed that by 5 min after internalization dead Salmonella-containing phagosomes (DSP) acquire transferrin receptors (a marker for early endosomes) while by 30 min the dead bacteria are found in vesicles carrying the late endosomal markers cation-dependent mannose-6-phosphate receptors (M6PR), rab7 and rab9. In contrast, live Salmonella-containing phagosomes (LSP) retain significant amount of rab5 and transferrin receptor till 30 min, selectively deplete rab7 and rab9, and never acquire M6PR even 90 min after internalization. Retention of rab5, rab18 and selective depletion of rab7 and rab9 presumably enable the LSP to avoid transport to lysosomes through late endosomes. Presence of immature cathepsin D (48 kDa) and selective depletion of the vacuolar ATPase in LSP presumably contributes to the less acidic pH of LSP. In contrast, proteolytically processed cathepsin D (Mr 17 kDa) was detected by 30 min on the DSP.

In order to quantify the transport of the live or dead Salmonella from the early compartment to the lysosomes, cells were preloaded with avidin-HRP and chased for 90 min to label the lysosomes. Subsequently, cells were pulsed with live or dead biotinylated bacteria at 37°C for a short period of time (5 min) to restrict their entry to the early compartment followed by a chase. At indicated times the formation of bacteria biotin-avidin-HRP complex was measured to determine the transport of the Salmonella to lysosomes. The results showed that dead Salmonella co-localized with avidin-HRP preloaded lysosomes within 45 min and maximum fusion was observed within 90 min. In contrast, live Salmonella did not form complexes with avidin-HRP even after 90 min.

We concluded that live Salmonella modulate the expression of various rabs (e.g., rab5, rab7, rab9 and rab18) on the phagosomes to reside in a specialized low acidity compartment devoid of active lysosomal enzymes and transferrin receptors.

Publications

Original peer-reviewed article

1.   *Hashim S, Mukherjee K, Raje M, Basu SK and Mukhopadhyay A (2000) Live Salmonella modulate expression of rab proteins to persist in a specialized compartment and escape transport to lysosomes. J Biol Chem 275:16281-16288 (*in press last year, since published).