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Monday Micro – Bioluminescent bacteria photobooth Siouxsie Wiles Apr 14

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For those curious how our bioluminescent photo booth went at Auckland’s Museum of Transport and Technology (MOTAT) recently, the results are up on Flickr. As a quick reminder, the light being used to illuminate the subjects was being supplied by glowing bacteria growing on large petri dishes. We used a 6 second exposure to take the pictures which has led to some interesting photos. Going by the number of blurry faces, I think it’s safe to say that most children can’t sit still for that long! Take a look and see if you recognise anyone. Here’s my favourite:

Jimmy

April’s Fool or just plain Fool? Siouxsie Wiles Apr 01

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The number of people who have died in Guinea from Ebola virus infection is now at 78, and Médecins sans Frontières says the country faces an unprecedented epidemic. Two sisters have died in neighbouring Liberia, one of whom had recently returned from Guinea, and Senegal has closed its borders with the west African country.

Despite there being no treatment or vaccine against this highly lethal virus, according to Joette Calabrese there is hope. “Fortunately for us, homeopathy has great renown for its healing ability in epidemics” she tells us.

In her blog post “Bioterrorism and Epidemics: Knowing Homeopathy Can Help Make the World a Less Scary Place” she writes: “The symptoms of Ebola and other hemorrhagic fevers resemble those of malaria, dengue fever, yellow fever and viral hepatitis. In homeopathy, remedies are often chosen based on the symptom picture, so the remedies most often used for Ebola will be the same as for these other diseases.” She goes on to list six homeopathic remedies which she says should be given every hour “…but as the severity of the symptoms decrease, frequency is reduced. If no improvement is seen after 6 doses, a new remedy ought to be considered”.

Reading Joette’s post on April 1st, I thought this must surely be a joke. But it seems not.

I’ll leave you with another useful product (AKA should be an April Fool’s gag), for those who are feeling a little run down and worried your diet might be lacking these core ingredients. One tablet daily is all you need, apparently.

Hat/tip to @zeno001, @cammerschooner and @nccomfort on twitter for these gems.

dna

Monday Micro – First documented cases of cat to human transmission of TB Siouxsie Wiles Mar 31

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A paper just published in the Veterinary Journal documents the first cases of transmission of Mycobacterium bovis* (the bacterium responsible for TB in cattle and many other species) to humans (1). Before anyone get’s into a panic, it was a year ago.

Alas, the article is behind a paywall, but according to the free abstract a vet practice in Newbury, in the UK, diagnosed nine domestic moggies with M. bovis infection between December 2012 and March 2013. The nine cats ‘belonged’ to different households** and six of them resided within a 250 metre radius. The animals presented with varying symptoms and severity and 6 were euthanased or died, while the three surviving animals were responding well to treatment. At the time of the article, no new cases had been detected in local cats since March 2013.

As people can become infected with M. bovis, Public Health England offered to screen 39 people identified as having come into contact with the infected moggies. 24 people accepted their offer; 2 people were found to have active M. bovis TB (this means they would be infectious), while another 2 people were found to be latently infected (and therefore not infectious). All are reported to be responding to treatment.

Molecular analysis has shown that the M. bovis isolated from the infected cats and people with active TB infection were indistinguishable, indicating transmission of the bacterium from an infected. The same strain has also been found in cattle from nearby herds, although according to Professor Noel Smith, Head of the Bovine TB Genotyping Group at the UK Animal Health and Veterinary Laboratories Agency, the cats are unlikely to have caught if directly from the cattle but from infected wildlife. He probably means badgers.

If you are curious how often cats are diagnosed with bovine TB in the UK, the Department for Environment, Food and Rural Affairs (DEFRA) have put up a spreadsheet with data going back to 1997 (the data for 2013 is provisionally as it only covers up to September). As you can see from the graph below, 2013 was far from the highest year. That honour goes to 2009 with 26 cases.

TB cats

It’s not just cats that have been diagnosed with M. bovis though. Pet dogs, pigs and even a few ferrets have had TB.

TB domestic

To put all these numbers in perspective, according to DEFRA the number of cattle compulsorily slaughtered in 2013 alone because they tested positive for M. bovis, or are direct contacts of positive animals, was 32,620. So the cats are really just a drop in the ocean. What this case does show though is just how versatile M. bovis is when it comes to picking a host. It also shows that we share our microbes with our pets, for better and worse.

And finally, an update on last week’s Monday Micro, the current Ebola outbreak in west Africa. The strain of Ebola responsible is Zaire, the strain most frequently associated with outbreaks and the one with the highest mortality. So far the total number of suspected and confirmed cases in Guinea has increased to 103, with 66 deaths, a mortality rate of 64%. Both Sierra Leone and Liberia have now alerted the WHO of suspected cases and deaths consistent with Ebola infection among people who have recently traveled to Guinea. The numbers for Liberia are 8 suspected cases, including 6 deaths, while for Sierra Leone it is 6 suspected cases, including 5 deaths.

Reference:
1. Gibbens N (2014). Mycobacterium bovis infection in cats. Veterinary Record 174:331-332 doi:10.1136/vr.g2344

*As an aside, the TB vaccine, commonly referred to as Bacille de Calmette et Guérin or BCG, is derived from a strain of M. bovis that was cultured in a laboratory for many years until it had lost some crucial genes that it needs to cause disease.

**Any cat owner will tell you its more like the other way around….

Monday Micro – Semen and the twitchy clap Siouxsie Wiles Mar 10

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Neisseria gonorrhoeae is the bacterium responsible for the sexually transmitted infection gonorrhoea, also known as the clap. Symptoms often include pain when peeing and a nasty discharge from your nether regions, although some people can be asymptomatic. The microbe isn’t hugely fussy about where it causes an infection, so you can also get gonorrhoea of the throat and anus if that’s where the bacteria are deposited.

Despite the fact that gonorrhoea can be prevented by using condoms, there are apparently more than 100 million estimated new cases worldwide each year. Unfortunately N. gonorrhoeae is becoming increasingly resistant to antibiotics, so researchers are trying to find out more about how the microbe is transmitted and exactly how it causes infection to develop new strategies to combat it.

Mark Anderson and colleagues have just published a paper in the open access journal mBio showing that various proteins in the fluid of semen makes N. gonorrhoeae mobile, through a mechanism called twitching motility. This is where the bacterium rapidly extends and retracts hairlike appendages found on its surface to make it move. The researchers also found that N. gonorrhoeae forms little microcolonies when exposed to seminal proteins, making it stick better to human cells. This work shows that the semen environment changes the bacterium to prime it for transmission between people.

In case you need an incentive to use a condom, here’s a movie of twitching motility in action, for another bacterium called Pseudomonas aeruginosa. So guys, you could have those little critters twitching around in your semen. Seriously. If you ever have a discharge, go see a doctor.

YouTube Preview Image

Reference:

Anderson MT, Dewenter L, Maier B, Seifert HS. 2014. Seminal plasma initiates a Neisseria gonorrhoeae transmission state. mBio 5(2):e01004-13. doi:10.1128/mBio.01004-13.

Where do all the women go? Siouxsie Wiles Mar 06

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This weekend is International Women’s Day and the theme this year is Inspiring Change.

According to the UNESCO Institute for Statistics, just 30% of science researchers are women. They have produced a nifty tool to see where those women work and in what fields.

UNESCO - Women In Science Interactive

For NZ, the tool says that 59% of Bachelors students are female, 51% of Doctoral students and 52% of researchers. Interestingly, when the researchers are broken down by sector, a whopping 67% of academic researchers are female, while only 25% of those in the public sector and 16% in the private sector are female. As I’m in academia, I’d really like to see the breakdown for faculty positions, as its my impression that there are much fewer women the higher up the academic food chain you go.

One of the many reasons put forward for this is that more men than women are invited to speak at academic meetings and that invitations like these are of great importance for academic advancement. So its interesting to see some data on this from Arturo Casadevall & Jo Handelsman. They have just published a paper in the open access journal mBio looking at the numbers of male and females speakers at American Society for Microbiology meetings.

Here are some of their findings from analysis of 216 sessions from 3 general meetings held in 2011, 2012, and 2013:
1. 104 sessions were convened by male-only convener teams
2. 112 sessions had at least one female in the convener team.
3. In sessions convened by all men, invited female speakers averaged 25%.
4. In sessions in which the convener team included at least one woman, woman speakers averaged 43%.

Inclusion of at least one woman among the conveners increased the proportion of female speakers by 72% compared with those convened by men alone.

Something to think about the next time you organise a seminar series or meeting.

Reference:
Casadevall A, Handelsman J. 2014. The presence of female conveners correlates with a higher proportion of female speakers at scientific symposia. mBio 5(1):e00846-13. doi:10.1128/mBio.00846-13

Monday Micro – mummies and ‘kissing bugs’ Siouxsie Wiles Mar 03

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The mysterious mummy in the Bavarian State Archaeological Collection

The mysterious mummy in the Bavarian State Archaeological Collection

For over 100 years, the Bavarian State Archeological Collection in Munich, Germany, has housed an unidentified mummy. No records remained of the mummy. Where had it come from? Who was it? How had the person died? Thanks to science, know we know.

To better understand the origin and life history of the mysterious mummy, researchers examined the skeleton, organs, and ancient DNA using a range of techniques, including CT scans, isotope analysis, and tissue histology. They have just published their findings in the open access journal PLOS One.

So what did the researchers find? By radiocarbon dating, the mummy originates between 1450 and 1640 AD, and examination of the skeleton suggests its of a female, likely to have been 20-25 years old at the time of her death. Analysis of fibres taken from her hair bands suggest they came from a South American llama or alpaca, while isotope analysis of nitrogen and carbon in her hair reveal she lived on a diet of maize and seafood. This and other evidence suggests a life spent in coastal Peru or Chile.

The mummy also showed significant thickening of the heart, intestines, and the rectum, features typically associated with chronic Chagas disease. Chagas disease is a tropical parasitic infection, caused by Trypanosoma cruzi and spread mostly by biting insects known as Triatominae. During the day, these triatomines hide in crevices in the walls and roofs, emerging at night to feed on sleeping inhabitants. Because they tend to feed on people’s faces, triatomine bugs are also known as “kissing bugs”. After they bite and ingest blood, they defecate on their ‘victim’. The parasites are transmitted in the faeces left near the site of the bite wound, which are transferred into the wound when scratched. The researchers found parasites in rectum tissue samples taken from the mummy which were positive for T. cruzi DNA.

But it wasn’t Chagas disease that killed the young lady. Analysis of her skull suggests she suffered a massive blunt force trauma to the centre of her face prior to her death, leading the researchers to speculate that she may have been the victim of a ritual homicide.

Reference:
Panzer S, Peschel O, Haas-Gebhard B, Bachmeier BE, Pusch CM, et al. (2014) Reconstructing the Life of an Unknown (ca. 500 Years-Old South American Inca) Mummy – Multidisciplinary Study of a Peruvian Inca Mummy Suggests Severe Chagas Disease and Ritual Homicide. PLoS ONE 9(2): e89528. doi:10.1371/journal.pone.0089528

Monday Micro – Microwave popcorn and Cystic Fibrosis Siouxsie Wiles Feb 24

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What on earth could link microwave popcorn and cystic fibrosis (CF), a life-threatening inherited disease most common among Caucasians? The additive 2,3-butanedione, also known as diacetyl, a volatile colourless liquid with an intensely buttery flavor.

Diacetyl is produced naturally as a fermentation product by some microbial species and can be found in some beers, as well as artificial butter flavourings and margarine. The US National Institute for Occupational Safety and Health has suggested that diacetyl, when used in artificial butter flavoring, may be hazardous. Workers in several factories that manufacture artificial butter flavoring have been diagnosed with rare lung disease called bronchiolitis obliterans (also known as popcorn worker’s lung). According to Wikipedia, Wayne Watson, a big eater of microwavable popcorn, was awarded over $7 million in damages in 2012, when a jury decided his lung disease was caused by the chemicals in microwave popcorn. In 2012, a paper published in the journal Chemical Research in Toxicology also suggested there may be a link between diacetyl and Alzheimer’s disease (1).

So what has diacetyl got to do with CF? CF is caused by a mutation in the gene cystic fibrosis transmembrane conductance regulator (CFTR), leading to a number of symptoms, including chronic lung infections, which often flare up requiring treatment with antibiotics. A paper just published in The ISME Journal reports that diacetyl was found in breath samples from CF patients and healthy controls, but at higher levels in the CF patients (2). The researchers suggest that the low oxygen conditions in the CF lung lead to fermentation by certain microbes, and the increased production of diacetyl. This may in turn cause other microbes to produce toxic compounds and further damage the lungs. The researchers are hopeful that monitoring diacetyl levels in CF patients may help predict flare-ups.

As an aside, I also just read an abstract for a paper (behind a paywall, alas) that claims to be the first description of a bacterial pathogen jumping from humans to plants (3). Andrea Campisano and colleagues report, in the journal Molecular Biology and Evolution, the discovery of a grapevine-associated relative of a bacterium that causes acne in humans, Propionibacterium acnes! They think that the bacterium jumped from people vines during the Neolithic period when grapevines were being domesticated.

References:
1. S S More, P Vartak, R Vince. The Butter Flavorant, Diacetyl, Exacerbates β-Amyloid Cytotoxicity. Chem. Res. Toxicol., 2012, 25 (10), pp 2083–2091, DOI: 10.1021/tx3001016

2. K L Whiteson, S Meinardi, Y W Lim, R Schmieder, H Maughan, R Quinn, D R Blake, D Conrad, F Rohwer. Breath gas metabolites and bacterial metagenomes from cystic fibrosis airways indicate active pH neutral 2,3-butanedione fermentation. The ISME Journal, 2014; DOI: 10.1038/ismej.2013.229

3. A. Campisano, L. Ometto, S. Compant, M. Pancher, L. Antonielli, C. Varotto, G. Anfora, I. Pertot, A. Sessitsch, O. Rota-Stabelli. Interkingdom transfer of the acne causing agent, Propionibacterium acnes, from human to grapevine. Molecular Biology and Evolution, 2014; DOI: 10.1093/molbev/msu075

Could dad’s-to-be drinking cause foetal abnormalities? Siouxsie Wiles Feb 19

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“Until now fathers’ lifestyle choices have not seen any repercussion on their unborn children. This ground-breaking research provides the first definitive evidence that fathers’ drinking habits pre-conception can cause significant fetal abnormalities.”

That was from a press release for a paper in a little known journal called Animals, Cells and Systems. The foetal abnormalities they are referring to are related to the spectrum of mental and physical defects that can develop in a foetus exposed to high levels of alcohol in the womb, known as foetal alcohol spectrum disorders (FASD). Present in an estimated 1 in 100 live births in the US, FASD is believed to be the leading preventable cause of mental retardation in the developed world. That is why women are strongly advised not to drink any alcohol during pregnancy.

But could FASD also be caused by dad’s-to-be drinking pre-conception? A group of Korean researchers set out to investigate this question (1). They took male mice and divided them into five groups. Four of the groups were given different amounts of alcohol, twice a day for 7 weeks, while one group weren’t given any alcohol. After the 7 weeks, they had a week off the booze after which they were placed with females for mating. The resultant foetuses were then examined towards the end of gestation to look for any differences in litter sizes, foetal weights, or for any abnormalities.

Here are the results:
For the low alcohol group (0.5g/kg), 1/8 litters had a foetus with abnormalities (1/120 foetuses = 0.8%)
For the mid alcohol group (1g/kg), 2/5 litters had a foetus with abnormalities (2/65 foetuses = 3%)
For the high alcohol group (4g/kg), 3/4 litters had a foetus with abnormalities (3/63 foetuses = 5%)
The abnormalities were pretty awful – brains growing outside of skulls, swollen brains and missing organs.

What interested me was, how much alcohol were the mice given in human terms? If we work on the basis of an 80kg man, the doses of 0.5g/kg (low) and 4g/kg (high) equate to 40 and 320g of alcohol twice per day for seven weeks, respectively. So how much alcohol is that? I turned to this great website to find out.

It turns out that a standard 330ml can of 4% beer contains approximately 10g of alcohol, as does a 100ml glass of wine. So the ‘low’ dose mice were drinking the equivalent of 8 cans of beer or 8 glasses of wine each day, for 7 weeks. To put this in perspective, the guidelines for men are 3 standard drinks a day and no more than 15 standard drinks a week (preferably with 2 days off a week). At 8 drinks per day, the ‘low’ dose mice were on 56 drinks per week. That’s nearly 4 times the recommended weekly amount.

So what about the ‘high’ dose? According to the website, a 1L bottle of spirits contains approximately 370g of alcohol, while a 3L cask of wine contains 300g alcohol. So the ‘high’ dose mice would be on something like the equivalent of a L bottle of spirits and 3L of wine each day, or 448 drinks per week. That’s nearly 30 times the recommended weekly amount. Imagine the hangover they had after 7 weeks! Actually, I’m very curious to know how the mice behaved while they were exposed to so much alcohol.

So while it certainly may be that dad’s-to-be should join their partners on the wagon while trying to conceive, I don’t think this study deserves the “groundbreaking research” tag trumpeted in the press release.

I chatted to Kathryn Ryan about this story on Radio NZ’s Nine to Noon Programme today, after I enthused about glowing cancer cells.

Reference:
1. Hye Jeong Lee, Jae-Sung Ryu, Na Young Choi, Yo Seph Park, Yong Il Kim, Dong Wook Han, Kisung Ko, Chan Young Shin, Han Sung Hwang, Kyung-Sun Kang, Kinarm Ko. Transgenerational effects of paternal alcohol exposure in mouse offspring. Animal Cells and Systems, 2013; 17 (6): 429 DOI: 10.1080/19768354.2013.865675

Meet the anti-vivisectionist Siouxsie Wiles Feb 16

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“Vivisection is scientific fraud” screeched the placard placed next to three elderly ladies sat on deck chairs. Attached to the fence beside them were pictures of caged monkeys and what appeared to be a dead dog. This was the scene that greeted passersby and staff and visitors to Auckland Hospital and the Medical School on Friday morning. I find protesters like these quite fascinating and am always interested to find out what they believe about the use of animals in scientific research. By the time I went to have a chat with them, a little drizzle meant only one lady remained, clutching another picture of a monkey and handing out leaflets produced by the NZ Anti-Vivisection Society.

“Do you know what they do in the basement of that building?” she whispered to me, pointing over at the university campus. Being a member of the Animal Ethics Committee (AEC), it turns out I do. The AEC is responsible for approving all research procedures carried out using animals, as well as regularly inspecting facilities. But I was curious what the protester believed. “Terrible, terrible suffering, and murder” she says. She quoted the National Animal Ethics Advisory Committee’s (NAEAC) figure of 301,964 animals used in scientific research in NZ in 2012.

I’m not surprised to find that the protester is cherry-picking data. Actually, those 301,964 animals were used for research, testing and teaching (RTT). Less than a third of those animals were used for biological or medical research, while a little more than a third were used for veterinary research. Over 80% of the animals were exposed to manipulations which had no, virtually no, or little impact on the animals’ welfare. To put this in context, breeding is considered a manipulation. More than 70% of the animals were returned to their normal environment afterwards. In other words, not “murdered”. Can you guess what the most used animal was for RTT in New Zealand in 2012? Cattle. They made up over half of those 301,964 animals. I can honestly say there are no cows in the basement of the med school. Given the protester was quoting NAEAC’s report at me, I asked her if she knew that no monkeys were used in RTT in NZ. “Yes”, she says. So isn’t it misleading to be displaying pictures of monkeys, I ask? “A little” she concedes. Might people passing by think that monkeys are being used in scientific research in NZ, I ask? “Maybe” she says. So she is not only cherry-picking but being downright dishonest too.

“That animals are made to suffer” was the protester’s main objection to the use of animals in research. I asked her if she has heard of the 3Rs* – replacement, refinement and reduction. These are the ethical and legal basis on which animals are used in research, teaching and testing in New Zealand and many other countries around the world. Animals should be replaced with an alternative if possible, but where not possible, the numbers used should be the minimum necessary, and procedures should be refined to cause minimal suffering. In reality, this means using things like pain killers to alleviate any suffering. “Nonsense” she snorts.

During our chat, I ask the protester whether she takes any medicines when she is ill and the conversation moves in an unexpected direction. I find out she believes the only causes of cancer are alcohol, smoking and doctors, and that there is no such thing as infection (“the bugs are just coming to clear up our mess”). Here I am on fairly strong ground, so I tell her I’m a microbiologist studying nasty microbes, and that many of them are not “clearing up our mess” but have entire systems devised to overcome our immune system and cause damage. “Nonsense” she snorts again.

I know this is not a popular view, but I would love to see universities being proactive when faced with protesters like this – perhaps putting up their own placards and talking to passersby about the benefits of research and the lengths scientists go to to minimise suffering. It is clear that we can’t change the minds of the die-hard protesters, especially those that believe you can avoid cancer by not visiting the doctor and that infectious diseases are a myth**. But I believe most people are curious and will listen to both sides of the story. By remaining in our ivory towers we are missing opportunities to engage with the people who stop and talk to the protesters, and those who see their placards. Instead we create the impression we have something to hide. We don’t.

*Not reading, ‘riting, ‘rithmatic, or reduce, recycle, reuse…

**I am not saying for a minute that all anti-vivisectionists are as crazy (in my opinion) as the lady I spoke to.

Monday Micro – killer viruses Siouxsie Wiles Feb 03

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Recent virus-related papers to get excited about:

1. Visualising HIV infection

A paper just out in the open access journal PLOS Pathogens describes using 3D electron microscopy to visualise the Human Immune Immunodeficiency Virus (HIV)-1 infecting gut immune cells (1). If you remember, HIV is the virus which causes acquired immunodeficiency syndrome (AIDS). It’s believed that 33 million people worldwide are infected with HIV.

Until reading this paper, I hadn’t realised that gut mucosal tissues were involved in HIV infection. According to the researchers, the gut contains large numbers of target cells which become depleted early on in HIV infection. Ladinsky and colleagues wanted to look at where the virus goes during an active infection so they needed to use some nifty tricks to make that possible. The first was to make mice which contain immune cells that HIV can infect. As the virus is pretty specialised for infecting human cells, it doesn’t normally infect mice. The researchers grafted mice with human immune cells, and then a few months later injected the mice with HIV. Mice were then euthanised and gut tissues removed and fixed for looking at using a fancy microscope. And here’s an example of a reconstructed image where the modelled virus particles are shown in blue. Pretty!

Tomographic slice of gut immune cells with modelled HIV virions (blue, membrane; purple, cores; average diameter = 99.3+/−4.7 nm). Adapted from ref 1

Tomographic slice of gut immune cells with modelled HIV virions (blue, membrane; purple, cores; average diameter = 99.3+/−4.7 nm). Adapted from ref 1

2. Hijacking the bacterial ‘immune system’ to make smart antibiotics

I’ve written before about the fact that bacteria can become infected with viruses, called phage. The bacteria have developed numerous forms of ‘immunity’ to protect themselves from attack, including the CRISPR system, which stands for Clustered Regularly Interspaced Short Palindromic Repeats. In this quite elegant system, foreign genetic material is chopped up and incorporated into the bacterial genome (as ‘spacers’) between CRISPR repeats. These spacers then serve as a sort of immune ‘memory’ of past potential invaders. Upon re-exposure, the CRISPR spacers recognise the foreign genetic material and target it for destruction.

In a paper just published in the open access journal mBIO, Gomaa and colleagues have shown that this CRISPR-Cas system can be hijacked to kill specific strains of bacteria (2). They designed and administered specific CRISPR spacers into mixed cultures of bacteria and showed that they could kill the particular bacterial strain they were targeting. This is exciting as one of the problems with current antibiotics is that they kill good and bad bacteria in one sweep. Now the researchers have to figure out CRISPR spacers could be delivered to target bacteria during an infection. Watch this space.

3. Exploiting viruses to target cancer cells for destruction.

And finally, a paper just published in the FASEB Journal describes using an engineered vaccinia virus to target breast cancer cells for destruction (3). Gholami and colleagues engineered vaccinia virus to carry the gene encoding the human sodium iodide symporter (hNIS). When the virus infected breast cancer cells, it made the cells produce hNIS. What’s cool about this is that hNIS is the protein that normally concentrates iodine in thyroid cells. By grafting the engineered tumour cells into mice, the researchers were able to treat the tumours by giving the mice radioactive iodine, a form of radiotherapy used to treat thyroid cancer in humans. Clever.

References:
1. Ladinsky MS, Kieffer C, Olson G, Deruaz M, Vrbanac V, et al. (2014) Electron Tomography of HIV-1 Infection in Gut-Associated Lymphoid Tissue. PLoS Pathog 10(1): e1003899. doi:10.1371/journal.ppat.1003899

2. A. A. Gomaa, H. E. Klumpe, M. L. Luo, K. Selle, R. Barrangou, C. L. Beisel. Programmable Removal of Bacterial Strains by Use of Genome-Targeting CRISPR-Cas Systems. mBio, 2014; 5 (1): e00928-13 DOI: 10.1128/mBio.00928-13

3. S. Gholami, C.-H. Chen, E. Lou, L. J. Belin, S. Fujisawa, V. A. Longo, N. G. Chen, M. Gonen, P. B. Zanzonico, A. A. Szalay, Y. Fong. Vaccinia virus GLV-1h153 in combination with 131I shows increased efficiency in treating triple-negative breast cancer. The FASEB Journal, 2013; 28 (2): 676 DOI: 10.1096/fj.13-237222

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