spiny-headed worms: interesting enough for round two

   To delve deeper into the spiny-headed worm story we must first understand the proboscis. The proboscis is a tubular body part that sucks. A butterfly’s tongue that sucks nectar out of flowers is a proboscis. An elephant’s trunk is often called a proboscis. And the spiny sucking apparatus of acanthocephalan worms is a proboscis. 

Close-up of butterfly proboscis (image credit)

   The proboscis in parasitic worms has two functions, to attach to the host and extract nutrients from the intestinal lining. The crazy thing about the proboscis in this particular group of worms is that it is biphasic; it can be tube-like and erect, or it can be flaccid and turn itself outside-in and retract within a compartment of the worm body. When R. A. Hammond started working on Acanthocephalus ranae, our spiny-headed worm friend from last week’s post, it was known that the proboscis could retract, or invaginate. What wasn’t known was how it actually happened. Thus, the goal of R. A. Hammond’s study was to identify the in-and-out mechanism of the proboscis. Let me just say here that up until this point I have tried not to use words suggestive of a penile erection. It is a little difficult because I am talking about a tube-like structure that swells and becomes erect to function, only to return to a flaccid state when not being used. But, it is important to understand that I am not avoiding this comparison because I am afraid to talk about genitalia; on the contrary, I talk about genitalia on a daily basis. I am avoiding this comparison because it is misleading. The main difference is that when a human (or mammalian) penis becomes flaccid it does not invaginate, it just goes limp. To invaginate, the tip would have to retract in on itself and rest within an internal receptacle. Interesting idea, right? This is how many animal penises operate, from insects to reptiles. Evagination for operation, invagination for daily life. Now that we have this out of the way, let’s move on.

   To figure out how the proboscis worked, Hammond used a technique first described by Pflugfelder in 1949. Pflugfelder! I am not going to go on a tirade about him, I want to focus on Hammond, but what a name. The technique involved feeding the parasite host, in this case the common toad (Bufo bufo), pork fat with a red stain dissolved in it. Once the fat/red stain solution was in the toad’s digestive system the parasites fed on it too. The stain was sequestered in particular structures of the worm called lemnisci, which were hypothesized to be involved with the evaginate – invaginate process. I know, lemnisci is not a term I use on a regular basis either, I’ll try not to let it contribute to confusion. To summarize, Hammond fed toads a fat/red stain mixture, dissected the intestines out of the toad, pulled out the worms, imaged the stained lemnisci under the microscope using still pictures and video, and traced the morphological changes from beginning to end. All of this to find out how the worm proboscis worked. Not to invent microneedles, not to develop a surgical adhesive, he wanted to know how it worked.

   What Hammond discovered was that the invagination and evagination mechanism was controlled by a set of muscles that pulled and pushed the proboscis into and out of the receptacle by changing the hydrostatic (fluid) pressure of various morphological components. Interestingly, once the proboscis was fully extended, a set of collar muscles around the base contracted and pushed fluid up into the proboscis wall causing the skin to swell. It was this swelling mechanism of the worm that inspired the microneedle adhesive.

Figure 1a from Yun Yang et al. (2013). Image caption: "Illustration showing mechanical interlocking of a water responsive shape-changeable microneedle following penetration into tissue."

I want to point out that the microneedle adhesives were inspired by the proboscis (bioinspiration) as opposed to mimicking the proboscis (biomimicry). The reason is that the swelling mechanism of the worm proboscis relies on muscular contraction whereas swelling of the microneedles occurs with the addition of water. What is similar is that they are biphasic, and have a tip that swells relative to a base that does not. A patent application for this discovery was filed on Nov. 26, 2015. Since the original publication describing swellable microneedles, there have been several other useful applications including designs to deliver drugs, vaccines, and insulin directly through the skin.

A side note: In light of what is going on with the water supply in Flint, Michigan, I wanted to also mention how P. laevis and its relatives can be used as bioindicators in freshwater ecosystems. Because P. laevis parasitizes freshwater fish, it has been shown they accumulate heavy metals, such as lead, from the aquatic environment and can be used to monitor heavy metal concentrations. Maybe we should send some to Flint.