EASTERN BIOLOGY NETWORK MEETING 12.3.02

SPEAKER: Dr Emanuela Handman, from WEHI.

Dr Handman’s area of specialisation is intracellular pathogens, especially parasites. She studies how they get into cells, how they live inside cells and what the host response is, as well as their survival strategies.

The host-pathogen interaction determines ‘who’s in charge’.

In general, if there is an infectious disease, all individuals may be exposed but only some will be infected, and of these only some will be diseased and even fewer of these will die – as genetic component to susceptibility to infection.

Dr Handman is studying primarily leishmaniasis but also to a lesser extent malaria at WEHI, and she talked to us more specifically on these diseases.

Note: AB = antibody, AG = antigen, RBC = red blood cell!

Malaria

Four pathogens:Plasmodium falciparum

P. vivax

P. ovale

P. malariae

All cause malaria, P. falciparum is the killer. These species are specific to humans. A significant component of the malaria research at WEHI by a large group led by Alan Cowman, Brendan Crabb and Louis Schofield are investigating the mechanism of parasite invasion of human red blood cells and the mechanisms which lead to the pathology caused by malaria. Mouse malaria is used as a model for the study of disease mechanisms but human malaria are used for the study of invasion. Unfortunately, the Plasmodia that infect other mammals don’t infect humans so there is no direct animal model for human malaria.

Complex lifecycles.

Parasites introduced by mosquito, move in blood to liver where they invade liver cells, but without producing symptoms. P. falciparum multiply asexually over about three weeks in humans then rupture the liver cells and move into the blood and infect RBCs. Reproduce extensively asexually then break out to reinvade more RBCs. Rupturing of the RBCs coincides with the symptoms. However, the precise mechanism and molecules involved in the pathology of disease are still not clear. Other types of Plasmodium can continue to survive in the liver and lie dormant for years (relapses). Upon immune suppression or trauma, these may surge and cause a relapse in disease.

The examination of the disease prevalence in an endemic population shows that babies are protected from disease through antibodies from their mothers, become infected at about three months of age, highest death rate at three to five years then prevalence drops; usually low in an adult but never zero. Although these individuals show no disease, they all harbour parasites despite having antibodies to them. Immunity is not sterile. Rise in prevalence in pregnant women, especially first pregnancy.

It is not possible to predict the onset or severity of malaria even though all hosts will have the parasites in their blood.

Two questions: how to the parasites evade the immune response of the host and what causes the disease manifestations in those individuals who do get the most severe form of disease, cerebral malaria?

How do the plasmodia evade the host response?

1. Antigenic diversity – there will be many variants of parasites in the blood. Like any population of organisms, they are not all alike. They may have a variety of distinct alleles of many of their genes. They are diverse.

2. Antigenic variationis the programmed expression of genes belonging to a family of about 50 VARIABLE genes encoding a surface protein which is exported by the parasite to the outside of the infected red blood cell. It is a flag that the parasite puts onto the host cell and it changes that cell drastically compared to the normal red blood cell. (see below).

Each parasite in the population expresses only one of these VAR genes and puts on to the RBC a unique member of the family. As the infected individual makes antibodies to the dominant VAR, the RBC expressing it will be killed and eliminated. However, new populations will expand over time. There is so much variation that individual people can’t build a sufficiently large bank of antibodies, ie enough immunity to protect against all the parasites, so some parasites survive.
This variation is one of the reasons why a vaccine difficult to make. The 50 or so genes that allow for AGic variation appear to be stable – no new ones seem to be appearing – worry that if a vaccine is developed, this will select for new versions.

3. Sequestration – the parasites stick to the capillaries so they bypass the spleen, where most of the destruction of the infected RBCs occurs. If the capillaries are in the brain, have cerebral malaria, the most severe form of the disease: the ‘killer malaria’.

In infected RBCs, the pathogen exports the product of the VAR genes to the RBC surface. The presence of this protein causes the appearance of knob-like protrusions on the surface and makes such surfaces ‘sticky’. (Mechanism is a research area – how do pathogens export whole proteins through several membrane layers? (Parasite in vacuole hence extra membrane layer)). Infection causes the production by the immune system of a protein called ICAM that makes the endothelium sticky too, hence the sticky RBCs containing the parasite stick to the sticky endothelium, initiating sequestration and reducing blood flow – may block capillaries.

Another study area is how cerebral malaria kills. The production of soluble cytokines calls all sorts of immune system cells into action. This is normally a very important defense mechanism, but when it is excessive, it may actually damage the host. One such example is septic shock syndrome. In this situation, the cytokine Tumor Necrosis Factor alpha is produced and it shakes up the immune system so much that it causes death. TNF-alpha is one of the cytokines that is up-regulated by infection with malaria. There is evidence that there is a correlation between the amount of TNF in the blood and the severity of disease. Polymorphism of TNF-alpha genes has also been shown to correlate with the severity of disease. There is a lot of work being done to understand the genetic basis of susceptibility to cerebral malaria because not all infected individuals develop cerebral malaria.

4. Immunosuppression – especially in pregnant women.

5. Rapid rate of reproduction

Other areas of research in malaria include the study of drug resistance, with the hope of developing new drugs.

Drug resistance has become a major problem; drug protection is no longer efficient, especially in Africa. A few new drugs are available, being used in combination therapy to reduce the chance of resistance – though still get some. Combination of drugs and public health measures are what currently available.

Leishmania major

It is a zoonosis; the host is a wild animal eg rodent or dog. Humans are accidental hosts. Means that have an animal model, unlike for malaria that is human-specific.

Macrophages are the main host cells, and dendritic cells. They internalise the protozoa by phagocytosis so they are inside membrane-bound vacuole (a phagosome), or more rarely in the cytosol. There can be more than one parasite / macrophage. Lysosomes accumulate nearby and fuse with the phagosomes but don’t digest the protozoans. The parasites have evolved mechanisms to avoid killing in the macrophage and trying to understand this is an active area of research. This is a similar interaction with a host to Mycobacteria (TB), except latter have thick and waxy cell walls and their mechanism of survival in the macrophage is by preventing the fusion of the phagosome with the lysosomes.

Intracellular replication – the parasites reproduce inside the phagocyte and are released by exocytosis – one host cell can release many leishmanias in a few hours.

Leishmaniasis is all round the world in tropical areas. It is not in Australia – yet – is now in East Timor.

Spread by sand flies. If cutaneous leishmaniasis, skin is eaten away (lesion). If visceral leishmaniasis, protozoans home in on liver, spleen and bone marrow. An important question in leishmaniasis is why do the different parasites migrate and home in on different organs to cause different diseases – do the infected macrophages migrate from the skin at the bite site? Or do the parasites move?

Invasion involves specific receptor-mediated interaction between the parasite and macrophage surfaces that allow the parasite to invade the macrophage. More than one molecule is involved from each, and alternative receptors are possible. This may explain how this parasite can infect humans as well as dogs or rodents.

Like in malaria, there is a genetic component to the ability of the host to resist disease, ie to be infected but asymptomatic. Genetic resistance is polygenic, ie it is due to the interaction of several genes – area of research, as is why some humans are resistant.

Ref handouts – one on malaria, one on Leishmanias – both detailed but interesting.

Our thanks to Dr Handman for an informative and interesting talk – and for her patience with questions!