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Show Notes
This is the second of several interviews we will do with significant contributors to the field of developmental bioelectricity. Min Zhao's work focused on the role of ion currents and applied electric fields in cell migration and wound repair.
https://scholar.google.com/citations?user=G7-zWBcAAAAJ&hl=en
https://health.ucdavis.edu/dermatology/faculty/zhao.html
Aastha Jain: https://www.livelongerworld.com/
CHAPTERS:
(00:00) Trauma surgery to bioelectricity
(05:19) Early bioelectricity discoveries
(13:58) State of bioelectricity field
(21:45) Becker and early pioneers
(32:46) Electric guidance experiments
(45:48) Three bioelectric research directions
(51:36) Fragment experiments and wrap-up
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Transcript
This transcript is automatically generated; we strive for accuracy, but errors in wording or speaker identification may occur. Please verify key details when needed.
[00:00] Aastha Jain Simes: thank you so much, Min, for taking the time.
[00:02] Min Zhao: Yeah. Well, thank you for having me.
[00:07] Aastha Jain Simes: We're excited to dig in and we can just get started. I know, Min, you started off with your work in trauma surgery as a physician. I'm curious if you can touch on your background and how you got interested in bioelectricity?
[00:25] Min Zhao: This is a long story. I was trained as a trauma surgeon in China after graduating from military medical school. I worked with one of the founders of trauma surgery in China, Professor Wang. At that time I mainly worked on what they call blast injury — explosives and severe damage — to see how that caused damage and how the tissue repaired. After that, I went to London to work with Jeff Bernstock in molecular biology and biochemistry at University College London. I thought I would go back to China to continue my clinical work, so I tried to look around for a job, looking for a project which was closer to clinical work. I found Professor Colin McCaig and John Forrest at the University of Aberdeen, and I went there. At that time, Colin was working on tissue regeneration of the central nervous system. He was using electric fields to guide neuron growth. John Horace was working on corneal wound healing. It was a perfect combination for me looking back. I combined electrical signaling with wound healing research, and it worked well. That's what brought me to electrically regulated wound healing. At the beginning, we were only trying to understand whether this is one of the factors in wound healing. Eventually, we found out that the electric signal can override other guidance mechanisms. That prompted me to think that this is not only one mechanism, but could be a predominant mechanism, maybe a conserved and ancient one. If you look at wound healing, you think about single-cell organisms, plants, or animals — from salamanders and other lower organisms to humans. We all heal wounds. The conserved key thing is the breakdown of the barrier between inside and outside. The immediate effect is communication between inside and outside. The inside and outside of the animal have chemical and electrical gradients. So this electrical breakdown of the barrier is the same mechanism for wounds in plants, in single cells, and across animal species including humans. This electrical communication might be the initial signal telling the organism that there's a breach of the barrier and that we need to repair it. When the barrier recovers and this communication stops, the wound electric current stops. At that time I thought I needed to move to a bigger place to understand the fundamental biology of it, and then to develop this, to use magnets to help wound healing. That prompted me to move to University of California, Davis. Even before that, Mike and I knew each other's work and we thought this really is a fundamental mechanism, not only for wound healing, but as Mike showed, for developmental biology, cancer, and many other areas of biology. This is a short journey of why I got here.
[05:19] Aastha Jain Simes: So we want to dive a bit into the history of the field. While we want to understand the history of the 1900s and how the field has developed, I know you've written a bit about some of the origins of bioelectricity as well, going back to Galvani's days. Could you touch a bit upon the origins of the field?
[05:50] Min Zhao: Mike is a much better person to talk about the origin of bioelectricity. Mike?
[06:00] Michael Levin: As you were developing your work in wound healing, I think your work in wound healing is quite unique. It's very different from what we do, and it's very different from what other developmental biologists who do bioelectricity in the field do. You can talk about what are the inspirations as you think about the bigger questions of how wound healing is controlled. Are the different types of wound healing that you find, for example, in amphibians and in mammals, the same? Are they different? What kind of background in that field informs your thought? How do you think about these things?
[06:51] Min Zhao: If we're talking about general wound healing in human skin or mammalian skin, this actually went back almost 200 years to Du Bois-Reymond, a German physiologist. He was the founder of modern electrophysiology. He measured action potentials. At that time it was not a single axon action potential, but a bundle of axons together, and if you stimulate one end, the action potential would propagate to the other end. He is the first one who discovered that. Almost at the same time, he tried to see whether there's any current flowing in and out of the skin breach or wound, and he found that. It is not a new discovery. If we go back to Galvani's time, with the cut nerve and a piece of frog skin, at the wound edge there would be this wound electric current. Galvani used this as a source. At that time, the understanding was very limited; he thought that this animal electricity was a kind of imaginary vitalism. Now we understand it's fluxes of ions. Tissue cells pump ions and generate and maintain this electric current. If we go back you can see that although our understanding is not as correct as it is now, the phenomena or the observation were there. They found out that wherever you breach an organism, there will be a flux of ions, eventually of specific ions. This is different from the electron electricity we use every day in our electronics and appliances, where the electricity generated by the power plant drives electron flows through conductive metals. In human biology, electricity is carried by fluxes of ions, like sodium and potassium. While the understanding is getting more detailed and scientific, the observation of electricity at wounds actually goes back hundreds of years.
[10:23] Min Zhao: As Mike just mentioned, if we look at the wound of a single cell—if you puncture a hole—do we have electricity at the wound, the primitive wound? We measure them, and other people measure it too. In the early days, about nearly 100 years ago, people used big axons: they made a cut and could measure the injury current flowing out and in. We know now that because you have a membrane potential, cutting it generates a current flowing in and out. With smaller preparations, like frog skin and tadpole skin, the same happens. If you make a wound, this flux happens and generates the electricity. In humans, electricity is generated on the same principle. This is the question I go back to from the early days when I started work with Colin McKay and John Forrester, and I always wondered whether this is true. Many other people questioned electricity—what it is and how it would happen at the wound. Is it really important? I kept asking myself too. If you look at an evolved multicellular organism, the barrier between inside and outside is always there. If the membrane is breached, the cell either reseals or dies. So this would be a cue or signal—so ancient in biology. I think evolution will take cues from nature and develop mechanisms to use this signal to heal. Biology can evolve and complex organisms originate. Specifically with skin or epithelial wounds, we have this electrical signal. But if you go back to the start of life, when breaches of membranes occurred, the flow of ions happened at the same time, intrinsically relating to electricity generation at the wound. I would think if biology didn't take that as a mechanism, it wouldn't go well with Darwinian evolution. Evolution will take any cues to improve survival, repair, and adaptation. That makes me believe this is a fundamental mechanism. Although we focus on wound healing, many other aspects of life would be hard to imagine ignoring this intrinsic aspect.
[13:58] Aastha Jain Simes: How would you describe the state of the field then in terms of the major thinking in the field, the experiments that were being worked on, or even the excitement around bioelectricity?
[14:25] Min Zhao: This field is like many other fields: sometimes it seems it developed quite fast and well. Sometimes you need to overcome many hurdles to get people to look in this direction. Sometimes I'm quite optimistic and sometimes I'm a little bit skeptical that it might take time for people to appreciate this mechanism. Specifically to the wound healing field, people tried to use electrode stimulation to enhance wound healing a long time ago and with many different approaches. The misconception is that you stick an electrode there and you would stimulate the wound to heal. But the biology itself is far more complicated than that. One of the arguments supporting the use of electricity in wound healing or regeneration is that it's cheap — a few hundred dollars — and you can stimulate the wound to heal. I think we need to think carefully about that statement. Nowadays, we know that if you develop a drug, you need millions of dollars to understand what is really happening in the biological system about this chemical. So if we just want to spend a much smaller amount of money to develop an effective therapy, that's not right. Also, because electrical stimulation is so easy to implement in a clinical context, although not correctly in most cases, people publish different results. Some say, "this is a magic treatment; a wound that never healed or had stayed there for many years healed after stimulation." Others say this doesn't really have any effect. If you think about the wound complexity, this is quite understandable: the wound is geometrically complex, chemically complex, and physiologically complex. This is a three-dimensional volume conductor. When we think about electricity, we usually have metal wires and electricity flowing in a direct direction from one side to the other. But in a 3D conductive medium the electricity goes every direction. This is much less well understood and very difficult to study. I think the promise is there, but at the same time the community and society need to understand that this is a new type of therapy and funding agencies need to spend time, money, and effort, rather than just think this is a magic thing — stick the electrode there and the wound heals. You only spend a few hundred dollars and the magic stuff will happen. We are starting to see funding boards become more willing to invest, but I would think there's still not enough.
[18:47] Aastha Jain Simes: Part of what you're saying is that initially when people started understanding that electrical currents could heal wounds, they thought there's some magic formula where if you just apply electricity, it's going to heal. But a lot of your work involves understanding how these electrical signals heal the wounds. It's a lot more complex than simply applying electricity.
[19:16] Min Zhao: As Mike's work already shows, this electricity is carried by ions, the charge carriers in biology. The ions: many different types like sodium, potassium, calcium, and chloride, and they can change. The biological system itself tries to control it in many ways, using ion channels, pumps, and tight junctions. The equivalents would be the battery, resistors, and transistors. This biological electricity needs to be understood first before we try to manipulate it. With advances in electronics, and with Mike leading the way, I think we will get a much better understanding of bioelectricity. I think the name bioelectricity is being punished somehow by charlatanism and magic claims—people making dead bodies move and seeing signs in it—but it's more than that. It's like Michael Faraday many years ago showed electricity and magnetism are connected by a swirling needle without touch. You start thinking, how can you actually make those things work together as a system? Biology found a way, and I think Mike is leading the way to understand the biology behind it, and not only for developmental biology, but it also offers a completely new understanding of other aspects of biology, including wound healing and regeneration.
[21:45] Michael Levin: What's your take on some of Becker's papers? Robert Becker made some striking claims about rat limb regeneration. He had quite a different model of how it worked. What do you think about that?
[22:13] Min Zhao: I think Becker's work is pioneering and quite important. It forms part of the foundation of our work now. But as I said, some of the understanding may not be as simple or as accurate as we hope or wish for. This needs to go in a parallel direction. First is to apply it as Becker's work, and others are trying to understand it, and they're going in parallel. At that time, the tools and the methodology were probably not yet able to really do this in a way that we can understand. We can still try that. Many things in medicine are just trial and error. For example, you try something that works and that's fine. Maybe if we understand it, that would be better. But if we don't understand why it works, let's do it. Nowadays, because we have developed such powerful mechanisms or technologies to understand things like Mike and other people are doing more and more now, I think we can understand more. For Becker's early limb regeneration repair work, what lacked was mechanistic understanding and a well-controlled approach that other people or other labs can easily reproduce and develop in a more scientific direction. I think now is a better time. When things developed at that particular time, we probably didn't have those techniques or technology to understand or to get better control.
[25:01] Aastha Jain Simes: On this point, who are some of the other scientists you drew inspiration from in the field or you built your work upon?
[25:15] Min Zhao: For the person I met, Lionel Jeffrey is certainly the one. I still remember when I was the junior postdoc in London and in Aberdeen; we met and I always got so excited about this work. He always said, "Calm down; you need to be able to explain things clearly and make other people excited." At the moment you become a scientist you're just a technician: you do nice experiments and get nice results, but it's very difficult for them. This is one example. He's a pioneer of the next level of the new era of bioelectricity and he did some pioneer work. I keep going back to read his papers. He's one. Later on I met Ken Robinson, Richard Nosatelli, and Richard Borgens. They all have contributed in many important ways to this field, including developing the technology to measure the wound electric field or any type of electricity associated with biological specimens. They measured the electric field at different types of wounds and laid the foundation for future work. There are other people who showed electrical phenomena, like Mooming Pooh; they were among the first to demonstrate that there is electricity in biological systems. You can measure and map them. Cells do respond to such electric fields. Another is Claudia Sten. This is probably more relevant to what Mike has been doing: using modern technology to map or measure electricity around developing embryos and see how that relates to the developmental process. Of course, Colin McKay and John Forrest observed this clinically in patients' eyes: the swirling movement of the epithelial layers in the cornea during the healing process. If this pattern is disrupted and the wound is not healing well, it raises questions about how this spatial movement pattern happens. There are many hypotheses, including electromagnetic guidance of cell movement. As Mike mentioned the Borgens' work, I haven't met them, but I know the work. Of course Mike's work is leading the way, and I read his papers again and again trying to understand. With my clinical background, I don't know genetics and molecular biology very well. I learned a lot of the molecular chemistry and understanding of genetics from his work. That work is the foundation and keeps inspiring me and my lab to push this forward.
[29:42] Aastha Jain Simes: I'm curious, do you know who the people working in bioelectricity were before Lionel Jaffe's era? As you said, Lionel Jaffe was the new era in bioelectricity.
[29:58] Min Zhao: At the beginning, when bioelectricity first emerged, people saw this magic effect: a piece of tissue twitch, a piece of muscle contract, the animal start to move and even the corpse move. The sensation was there, but the real development came with Michael Faraday's discovery showing that a needle, without touching it, started to move. Michael Faraday's work revolutionized society. Now we see it everywhere. Without him, we would not be here. And then James Clerk Maxwell really connected electricity with everything. And as Einstein said, James Clerk Maxwell is a giant; he stood on the shoulders of others and developed the theory of relativity. So those are also great people underlying our hope that human society moves forward. I forgot what you asked. Sorry.
[31:45] Aastha Jain Simes: I was curious who some of the pioneering scientists were before Lionel Jaffe, but I think you answered it.
[31:54] Min Zhao: It was in a more broad sense. In biology, there are many other, as Mike mentioned, more clinically relevant people like Becker, and he's a clinician and tried many things. But it's hard when people look at more fundamental biochemistry, genetics, and cell biology. Now I think it's a good time that bioelectricity gets more connected with the traditional understanding of biology itself.
[32:46] Michael Levin: Do you want to go through a few examples? Your work is really extremely impressive and very close. I think maybe you're the closest to clinical application in this field. I'm just curious if you could go through a few—skin, cornea—you've done some amazing things. So what are some of your favorite stories so far that have come out of your lab?
[33:11] Min Zhao: This can go a little bit further in detail. When I left London to University of Aberdeen in very north of Scotland, I was thinking that maybe after a few years and I finished my postdoc training, I would go back to be a trauma surgeon again. I remember the first thing is the cell movement in the electric field is so dramatic. At that time when I talked to the people in the lab I said, we don't have a video recorder, we don't have a computer recorder. What I did is that I took a photo at different time points, like 0 hour, one hour, two hours. I printed them out on photo paper and compared them to see whether they moved. The first experiment worked, and I saw the cells move directionally. I was so excited. That made me stay there a little bit longer. Then we started to ask, well, at the wound there are so many mechanisms we accept that stimulate and guide the cell into the wound to heal. Now you say electricity and how important this is. There was a postdoc in my lab. We tried to make a wound and apply an electric field across. At that time we started to have the video recorder. We could see the wound edge move. For example, this is the wound, this is one side of the wound, the other side of the wound. What people normally do is to measure the area in the middle of the wound and to see how the wound becomes smaller. After a few months, she never told me the result. I kept asking her and it turned out that she thought that I wanted to see the wound getting smaller. Her result was that when she applied an electric field across the whole field, and one side moved, the other side moved away. So the wound area didn't really become much smaller than the control, because the control wound actually moved in and healed. She was quite hesitant to tell me the result. I said, after this two or three months' experiment, I would like to see the result.
[37:22] Min Zhao: She brought the video to me and I started to see one side moving under the guidance of the electric field, the other side being guided away. I said, "Wow." It looks like this is more important because at this experimental wound we have all other accepted guidance cues, but applying this electric field overrides them. One side actually moved away, and this was more important than I thought. I said this does not just make it go smaller; they actually override the guidance mechanisms like injury stimulation, contact inhibition release, population pressure growing into the wound, or the chemical release at the wound to attract the cell. This is not just one of the mechanisms. It seems that it overrides and is a predominant or master signal guiding and mobilizing the cell into the wound. At that time I started thinking about this. At the wound you have so many different chemicals like growth factors. You could have hundreds of them. If you add each of them there, you will see some effect. But none of them are able to really make this piece of tissue move away or in as you change the guidance direction. We asked whether the electricity that causes such an effect is physiological. We looked into the literature and saw measurements from Ken Robinson's lab, Lucitelli's measurement, and Richard Bogen's measurement. The field strengths are within those measured in vivo at wounds. So these physiological electric fields are able to produce this overriding guidance effect. I started thinking maybe this is not just one mechanism. It could be a predominant or master signal to mobilize and guide the cell, at least in a simple wound-healing model. We tested in an organ culture system and this still showed the same effect. That made me more excited. We talked about the fundamental mechanisms, and this experiment made me think this could be a very important mechanism. This was kind of a second discovery. At that time, nobody was able to use other guidance mechanisms like chemotaxis or durotaxis to cause massive cell movement. I think I remember well what came out of the lab. Then we started thinking about the many genetic and molecular mechanisms that regulate cell movement.
[41:33] Min Zhao: Does this electric field or electric guidance actually use those mechanisms or intersect with those genetic and molecular magnets? I start to get in touch with Peter Devreotes at Johns Hopkins and Henry Bond at UCSF and Joseph Penninger at that time at the University of Toronto, because they all study this chemotactic effect and they use a molecular and genetic approach to see how cells migrate directionally in chemical gradient. At the beginning, when we contacted them about this electric-field-guided cell migration, they were very skeptical and were thinking, what electric field? Others were Vick Small in Vienna and I was in Scotland, closer in distance. They were trying to do similar experiments. It's very hard to repeat because most of the lab members are trained in biochemistry and molecular biology; they are very good. They are leading experts at manipulating chemicals. But electronics is less familiar to them, so in the lab it's difficult to repeat. I said I can come over to do the experiment in your lab. I went there and we reproduced this electric-guided cell movement and then we started to use a different model organism like Dictyostelium. We knocked out genes, and with neutrophils in Henry Bond's lab we blocked a certain signaling pathway. With Joseph Penninger, he had the expertise to knock out genes in mice, and we could use these cells and tissues to test and see how the cells actually sense or transduce this electrical signaling into directional response. At that time we found that key molecules like PI3 kinase and PTEN, important intracellular signaling mechanisms, participate in this electrical-field-guided cell migration and in wound healing. With their help, we started to understand more about these important mediators or molecular magnets underlying electrically guided cell and tissue movement and wound healing. Those are the early experiments I remember in the lab; they bring back a lot of good memories of working in different places and with different people. People started very skeptical and later became very enthusiastic. Peter Devreotes and I are still working together trying to understand how, for example, cells are in an environment with a chemical environment, a mechanical environment with Wolfgang Losert at the University of Maryland, and also an electrical environment. How the cell integrates them into a behavior response—although we are able to understand them separately one by one, the integration is key. We're not there yet, but probably with this integrated approach we'll eventually be able to combine biochemical, biomechanical, and bioelectrical factors to see how cells collectively make a decision and respond to diverse environmental cues. Donald Ingber is another person who inspired me. I remember we spoke at a meeting and he said, don't keep going. At the beginning when he was working on mechanical things, people were always wondering how mechanical forces out there and chemicals and signaling in the cell interact when you're talking about mechanical aspects. He's a big source of inspiration for me as well.
[45:48] Aastha Jain Simes: What are some of the questions that you are exploring currently?
[45:57] Min Zhao: When I moved the lab to the US from the UK, I was thinking there are three directions I would like to pursue. The first is that we talk about the wound, we can measure the electric field. How the wound actually produces such a field and regulates it. We know that our tissue, or the wound, is composed of cells; the cells form tissue and have ion channels and pumps, and those ion channels and pumps, together with the tight junctions, form a biological electrical circuit. This circuit actually generates this electricity, and it comes into being when the barrier is broken down. When the wound heals, it disappears. So a fundamental question is how the wound actually produces and regulates such a signal to best achieve wound healing. We're trying to see whether we can find what we call the molecular generator, like a little power plant in the tissue that actually generates this electricity in response to injury. This is one direction. The other direction is how the cell actually senses such an electric field. This is a long-standing question, and many people in the field are working on it. When I first saw the cell movement, I talked with traditional electrophysiologists. Very disappointing to me was that most people said they wouldn't do anything because the field is so weak. They argued that to induce an action potential you need a much larger, stronger field, and that wound fields wouldn't do anything. But if you look at videos of cell movement during wound healing, the cells certainly respond to it. Working with Joseph Penninger, Henry Bond, and Peter Davoutis, we discovered some of the important molecular and genetic elements. We have not found a sensor yet. For example, we can see light.
[48:45] Min Zhao: Light is electromagnetic waves and our retina detects them and we can start to see them. The cell senses it. But for such a small DC-natured electric field, we don't know what the sensor is. We have some clues, we have some indications, and we found out some of the mediators. But the sensor has largely been elusive. This is another direction we're trying to see whether we can eventually find the sensor. I'm thinking about Donald Ingevers saying how the cell senses mechanical force. One of his words is that the whole cell is a sensor. That could be true. The whole cell senses it as a unit. It's not the traditional way, like a molecule as a ligand sensing it. The sensor could be more complicated than a single molecule. It could be a set of molecules. It could be the cell as a sensor. We're still working with Peter Davotis, and we're trying to manipulate genetically the molecule to see whether we can find the sensor. The third direction is working with Marco Rolandi and other colleagues from Santa Cruz and Riff Isarov, a clinician-scientist here at UC Davis, and together with Mike, we're trying to see whether we can develop some treatment to precisely regulate the wound electricity and deliver chemicals electronically to help wounds heal. Even if we don't fully understand the mechanism — how the cells sense the electric field, how the wound generates an electric field — we can possibly develop technology to enhance wound healing while at the same time trying to gain more fundamental understanding. Those are the three directions my lab is pursuing.
[51:36] Michael Levin: One of my favorite papers of yours is the one with the first author Sun, where the entire cells go one way in an electric field, and if you fragment them into pieces, all the pieces go the other way.
[51:52] Min Zhao: That was incredible. I remember this experiment was conceived many years ago before we were actually able to do it. I remember I tried it with Henry Bone. This was back in Aberdeen when I saw a paper about cell fragments. A fragment of a cell means that the cell doesn't have a nucleus, just part of the cytoplasm called a fragment. This has biological significance — platelets are such a kind of structure. Exosomes are membrane so-called structures with a little bit of cytoplasm inside. What Mike mentioned is that neutrophils actually release part of this cytoplasm as a little particle or little fragment to combat infection. I went to his lab and I tried to do that experiment. It turned out it's quite difficult to get enough cell fragment from neutrophils, so we were never able to get a conclusive result. Later, when we were in Aberdeen, Julie Thiart's lab — the other group showed that fish keratocytes are very big. When you treat them with certain chemicals, part of the cell body comes off, and this little fragment is still able to move around. We thought this was a good example. Together with Alex Mogila, who at that time was at University of California, Davis and later moved to NYU, we talked with Dr. Sun and they said, let's culture the cells to generate this fragment and put them in an electric field. The result was something we never expected. The fragment that came off actually moved in the opposite direction from the mother cell. It looks like the sensor and the response and decision making are different parts of the whole process. The cell can sense an electric field and the cell can respond to it. But the cell also can make a decision whether to go left or right, to the anode or to the cathode. This makes me think more about what Donald Ingeverse was saying — maybe the whole system is a sensor. It doesn't use a single molecule as a sensor that responds; it's coordinated and makes the decision to go to the cathode or to the anode. Thank you, Mike, for bringing up that really mind-boggling experiment. We could never have guessed the result would be like this. We would have thought the fragment would move together with the mother cell, but no — they moved in opposite directions.
[55:50] Michael Levin: For me, we spend a lot of time thinking about collective intelligence and how the preferences of the collective emerge from the preferences of the parts, how the scaling works. And here you showed us a great example where the parts have a certain preference, but the collective, once you put them together, the collective actually has a quite different preference for its action. So I think that's a powerful example. Well, thank you. Thank you so much. This is a real pleasure. Min Yu and I have known each other for a long time, but I think your work is amazing. I think it's the closest probably to the clinic of any of us in the field right now. It's beautiful.
[56:32] Min Zhao: Wow, thank you so much.
[56:34] Aastha Jain Simes: Thank you so much, Min. Really appreciate you taking the time. This has been amazing.
[56:38] Michael Levin: Yeah, much appreciated.
[56:41] Min Zhao: It's a great pleasure. I hope this field keeps moving forward and someday we'll see a new horizon.
