In vitro reconstitution of intracellular transport: Role of GTPases

 
Principal Investigator :  Amitabha Mukhopadhyay

Project Associates/Assistants
Seema Bhatnagar

Ph D Students
Sudha Bala Singh
S Parashuraman
S Senthil Kumar
Ganga Krishnamurthy
Shruti Aggarwal

Pathogenesis is related to the survival of pathogens in macrophages. The main goal of this project is to understand the mechanism of survival of pathogens in macrophages. We have also initiated the studies to understand the hemoglobin trafficking in Leishmania using in vitro reconstitution experiments. 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 this part of present investigations are (i) reconstituion of in vitro fusion of phathogen-containing phagosomes with early endosome to understand the interaction between these two compartments, (ii) modulaton of phagosome and endosome fusion by pathogens, and (iii) determination of the role of various signal transduction intermediates in the phagosome endosome fusion. Secondly, evidences from a variety of sources, have established that transport of cargo along the endocytic pathway requires a series of highly coordinated and specific vesicle fusion events regulated by small GTP binding proteins of the Rab family. Not much is known about the regulation of endocytosis and intracellular trafficking in protozoan parasites. The major objective of this aspect of the project is to understand the role of GTP binding protein in hemoglobin trafficking in Leishmania.

Mechanism of survival of Salmonella in macrophages

In the reporting year, we have further characterised the intracellular route of wild type Salmonella dublin (strain 2229) and SopE knockout mutant Salmonella dublin, (strain SE1) in macrophages to determine role of SopE. Initially, we have shown that SopE mediated recruitment of Rab5 from the host cell on phagosomes promotes fusion with early endosomes. Our recent results have shown that SopE knock out mutant Salmonella-containing phagosomes unable to fuse with early ensosomes and thereby targeted to compartment which is positive for Lamp1 and contains mature cathepsin D, a lysosomal enzyme suggesting that SopE knock out mutant is targeted to lysosomes like a dead bug. These results unequivocally demonstrated that SopE probably is the major player in the survival mechanism of Salmonella in macrophages.

Recent studies have shown that Rab GTPase, localized on specific compartment activate a pair of SNARE, v-SNARE and t-SNARE which further regulate the transport between the specific compartment. Accordingly, studies were initiated to determine the role of SNAREs in the maturation of Salmonella in macrophages. Earlier, we have shown that fusion between early endosomes with early Salmonella-containing phagosomes are sensitive to ATP hydrolysis and NEM treatment. However, recent results have shown that fusion of early endosome with late phagosomes is not inhibited by ATPgS and NEM treatment suggesting SNAREs are possibly activated on phagosome during maturation. To determine the role of different SNAREs, we have cloned and expressed different early and late endosomal v-SNARE and t-SNAREs, namely Syntaxin 7, Syntaxin 13, VAMP 7, VAMP 8. We have used the specific antibodies against these and other SNAREs to determine the relative level of these regulatory molecules on early and late Salmonella-containing phagosomes. Our preliminary results suggest that Syntaxin 6 and Syntaxin 13 are recruited more efficiently on late-Salmonella containing phagosome in comparison to early phagosomes.

Mechanism of hemoglobin trafficking in Leishmania

Small GTP binding proteins of Rab family regulate intercompartmental transport through a series of vesicle fusions. The early events in endocytosis are regulated by Rab5 whereas Rab7 serves as a targeting signal to late compartment. In the reporting period, we have cloned and expressed Rab7 homologue from Leishmania. Using specific antibodies against Ld Rab7, we have shown that Rab7 in Leishmania promastigotes localizes in perinuclear late endosomal compartment. To determine the role of Rab5 and Rab7 in hemoglobin trafficking in Leishmania, we have compared the fusion of Hb-containing early endosomal compartment with early or late compartment containing fluid phase marker.

Our results showed that fusion between early endosomes was inhibited by about 75% in Rab5 depleted cytosol, whereas Rab7 depletion reduced fusion by only about 25%. Addition of in vitro prenylated LdRab5 to the Rab5 depleted system completely restored fusion to the control level. Previous studies have shown that early endosomes can fuse with early endosomes whereas in vitro fusion between early and late endosomes does not occur. This prompted us to test heterotypic fusion between early and late endosomes in Leishmania. Accordingly, late endosomal fractions were prepared by 5 min internalization of AHRP followed by 15 min chase at 23°C as described previously and separated by sucrose gradient. Partial characterization of fractions containing maximum HRP activity revealed that these vesicles predominantly contain Rab7, a late endosomal marker, but no Rab5 or transferrin receptor, whereas, 5 min internalized AHRP vesicles possess early endosomal markers like Rab5 and transferrin receptor. In contrast to the previous study, about 80% fusion between BHb-loaded early endosomes and late endosomes containing AHRP was observed in Leishmania. However, consistent with the earlier report, that early endosomes containing fluid phase markers like avidin and BHRP fuse efficiently whereas fusion of early endosomes containing avidin with late endosome containing BHRP is significantly inhibited. Moreover, the observed heterotypic fusion between BHb-loaded early endosomes and late endosome containing AHRP is significantly inhibited in the presence of Rab7 depleted cytosol but not by Rab5 depleted cytosol. Addition of in vitro prenylated LdRab7 to Rab7 depleted system significantly restored fusion. These results indicate that the cytoplasmic tail of HbR from early endosomes containing BHb may possibly promote this heterotypic fusion.

To determine the role of cytoplasmic tail of HbR in heterotypic fusion, we have cloned and expressed different deletion mutants of the receptor as GST fusion proteins : the N-terminus (HbR-DC), middle region (HbR-DNC) and C-terminus (HbR-DN). Our results have shown that polyclonal antibody against Hb receptor purified from Leishmania (PHbR) recognized HbR-DNC and HbR-DN while a monoclonal antibody (1B6), specifically recognized HbR-DN. In addition, HbR-DC predominantly bound with Hb in comparison to other fragments. When BHb-loaded early endosomes were pretreated with 1B6, heterotypic fusion with late endosomes containing AHRP was significantly inhibited. Moreover, addition of HbR-DN in the fusion assay inhibited about 80% of fusion, whereas no significant inhibition was observed with HbR-DC or HbR-DNC.

Publications

Original peer-reviewed articles

1.     Singh SB, Tandon R, Krishnamurthy G, Vikram R, Sharma N, Basu SK and Mukhopadhyay A (2003) Rab5 mediated endosome-endosome fusion regulates hemoglobin endocytosis in Leishmania donovani. EMBO J 22:5712-5722.

Reviews/Proceedings

1.     Mukhopadhyay A and Basu SK (2003) Intracellular delivery of drugs to macrophages. Adv Biochem Eng Biotechnol 84:183-209.