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Tracing mad cow to human infection

Case research maps how illness makes cross-species jump
 

By John Mangels
Plain Dealer Science Writer

Monday, April 19, 2004

New research by Cleveland scientists may help explain how the infectious proteins implicated in illnesses such as mad cow disease are able to penetrate the natural barriers between species.

The study, by Case Western Reserve University researchers, shows it is relatively easy for a mammal protein called a prion to morph into a stealthier strain capable of outwitting the species firewall.

All it takes is exposure to a fragment of an abnormal prion protein from a third species, a process called "seeding," the Case team reports in the current edition of the journal "Molecular Cell."

The new prion strain has the same chemical fingerprint as before, but a different three-dimensional shape. This altered profile is like a fugitive's disguise.

Apparently, the altered profile is what enables the rogue prion to escape recognition and slip past the defenses meant to stop species from swapping illnesses.

Scientists have suspected such a process allowed sheep-tainted cow prions to infect humans beginning in England in 1995. But they lacked a molecular model demonstrating how prions might have created new strains, enabling them to jump the species barrier.

The Case study provides that, several prion experts say. Along with similar recent research in yeast, it also largely rebuts the long-debated idea that something other than or in addition to a prion - a virus, perhaps - causes the family of mad-cow-like illnesses in animals and humans.

The Case experiments were done in test tubes, using prions from mice, hamsters and humans. The study's authors caution that they have not yet determined if the outcome would be the same in lab animals, whose biology is much more complex.

"There might be other components in the body that . . . make it much more difficult for those [species] barriers to be crossed," said senior author Witold Surewicz, a professor in Case's department of physiology and biophysics.

Still, the prion's surprising ability to adapt and exploit a weakness in the species barrier has major implications for the further spread of disease that policy-makers shouldn't ignore, concluded the authors and several other scientists.

"The bottom line is, if we don't tightly control these diseases, we're going to regret it big time," said Dr. Pierluigi Gambetti, director of the National Prion Disease Pathology Surveillance Center at Case. They "may come in through the back door."

Gambetti, who was not involved in the study, is a member of the U.S. Food and Drug Administration advisory committee on mad cow and related diseases. He and others strongly advocate expanding the government's cattle-testing program, which currently is limited to animals showing signs of illness.

A common cause

Researchers have known for decades of a seemingly related group of diseases that progressively destroy brain tissue, causing dementia and death in animals and humans.

The maladies strike hamsters, cats, sheep, cattle, deer, elk and people. Some are inherited, others infectious (an epidemic of the brain-wasting illness called kuru in the 1900s stemmed from New Guinea cannibals eating their infected relatives). Still others appear to occur spontaneously.

Only in 1982 did University of California, San Francisco, researcher Stanley Prusiner propose that the brain-wasting diseases had a common cause: a misshapen protein he'd found in the brains of diseased hamsters. He called it a "prion," a rough abbreviation of "proteinaceous infectious particle."

It was a radical notion, this idea that a nonliving speck of chemicals could malevolently transform other prions, thus spreading within and between bodies like an invading army.

Proteins, after all, are simpletons, nothing but long chains of amino acid molecules folded into elaborate three-dimensional shapes that resemble the bows on birthday presents. Unlike the traditional couriers of disease, proteins lack the genetic instructions for copying themselves. They can't split like a bacterium or hijack a cell's replication machinery like a virus.

So how could a prion protein, which normally perches harmlessly on the surface of a nerve cell, turn deadly and recruit its colleagues to wreak havoc in the brain?

Prusiner theorized that something initially caused a normal prion protein in an animal or human to refold into a harmful configuration. When this rogue came into contact with a normal prion protein, it latched on and bullied its impressionable partner into matching its aberrant shape. Gradually, lots of these individual conversions resulted in dark, gummy clusters of prions, rendering the brain a spongy mess.

Questions linger

Prusiner won a 1997 Nobel Prize for his discovery, but many questions remained. Two were especially troubling:

How could prions made of the same amino acid ingredients, arranged in the same order, form different strains that vary in infectiousness and symptoms? It would be like being able to brew cups of Earl Grey and orange pekoe from the same tea bag.

Since different prion strains had the same amino acid sequence, why didn't species barriers keep them all out? Researchers had thought the barriers worked primarily by reading prions' amino acid sequences, like a bouncer checking patrons' driver's licenses. If that were true, none of the prions should get in, since in effect they all had the same bad ID. But some clearly sneaked past, as evidenced by the outbreak of mad cow disease in humans beginning in the mid-1990s.

Scientists suspected the answer to both questions had to do with the invading proteins' altered shape, and that the shape - and thus the strain - evolved as prions passed through multiple species.

The Case team devised a test. They took mouse prions - which because of species barriers shouldn't be able to corrupt hamster prions - and "seeded" them by exposing them to a highly purified bit of infectious hamster prion.

The seed was so small, it didn't change the mouse prion's overall amino acid sequence - its molecular ID. But it was enough to cause the mouse protein to start acting like a renegade hamster prion, capable of bullying other hamster prions into refolding.

So the seeding must have caused the mouse prion to reconfigure its three-dimensional shape. The experiment showed prions with the same sequence could fold in more than one way, with different properties, like a Swiss army knife that can transform itself into a can opener, scissors or screwdriver.

By changing the mouse prion's shape, the Case researchers had created a new strain and enabled it to cross the species barrier.

Public health implications

The barrier, then, must rely more on shape recognition than onthe prion's amino acid sequence. It can be fooled by shape differences, just as a bouncer might turn away underage guys but admit an attractive girl even though her ID shows the same birth date.

"It is reasonable to feel a little less safe," said Dr. Neil Cashman, a neurologist at the University of Toronto's Center for Research in Neurodegenerative Diseases. "This study points up the fact that our previous reassurances are wrong. But it also provides a signal that much more science is needed. There are many things we don't understand, and the whole science of how prions propagate and cross species barriers is developing as we speak."

Assuming the Case findings can be verified in lab animals, several researchers said they are concerned that new prion strains may appear and spread in the manner the study demonstrated.

For example, sheep prions aren't known to be infectious to humans. But that could change if they were seeded by exposure to an abnormal cow prion passed along in contaminated feed.

"We need to be considering all these events very, very cautiously," said molecular biologist Giuseppe Legname, who is part of Prusiner's research group in San Francisco. "It's important that better screening be put into place so that what ends up on our plates is a safe product. I'd rather be safe than sorry."

Although the research is sobering, Surewicz - one of the study's authors - and others say it could also lead to drug strategies that stop the prion from refolding into a harmful shape.

"We don't understand the process of conversion, but the normal form has to be reinforced," Cashman said. "It's conceivable there are medicines that may bolster it, rigidify it."

To reach this Plain Dealer reporter: jmangels@plaind.com, 216-999-4842