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Journal Club Theme of June 2013: Biological Ferroelectricity: from Speculation to Reality

jiangyuli's picture

When a dielectric is placed in an electric field, it becomes polarized - positive and negative charges are separated, producing polarization defined as dipole moment per unit volume. Simultaneously, the dielectric experiences electrostrictive strain that is quadratic to polarization, though it is usually negligibly small. However, if the dielectric has no symmetry center, relatively large piezoelectric strain proportional to the electric field is also possible. Among 21 crystalline classes without a symmetry center, 20 of them are piezoelectric, within which 10 of them possess a unique polar axis that is spontaneously polarized, referred to as pyroelectric, whose spontaneous polarization varies with temperature. If such spontaneous polarization can be reversed by an external electric field, then the pyroelectric is also ferroelectric, and ferroelectricity refers to switching of spontaneous polarization in pyroelectric.

The history of ferroelectrics can be traced back to 1655, when Rochelle salt was first separated by Elie Seignette in France. But it was not until more than 200 years later that the piezoelectricity of Rochelle salt was established by Curie brother in 1880. It took another 40 years for the hysteretic nature of polarization demonstrated in Rochelle Salt by Holland graduate student Joseph Valasek in 1920, who coined the term ‘ferroelectric’ to reflect its analogies with ferromagnetism. During the Second World War, piezoelectricity and ferroelectricity were discovered in barium titanate and other perovskite oxides, and many technological applications emerged.

Piezoelectricity in biological system was noticed first in 1940. When wool fibers are rubbed together, the sign of triboelectric charges produced depends on the sense of rubbing; A.J.P. Martin attributed such phenomenon to pyroelectric and piezoelectric effects [1]. Former Soviet Union physicists observed piezoelectricity in woods in early 1950s, and Eiichi Fukada published a landmark paper in 1957, reporting piezoelectricity in bone [2]. Many biological tissues were proven piezoelectric afterward, leading to speculation that piezoelectricity is a fundamental property of biological tissues [3]. Not long after the discovery of biological piezoelectricity, pyroelectricity was reported in bone and tendon by Sidney Lang in 1966 [4], and subsequently in many other biological systems [5], leading to speculation of biological ferroelectricity as well [6]. However, it took almost 50 years for such phenomena to be reported experimentally.

There are actually fascinating theories on biological ferroelectricity in ion channels, hypothesizing conformational transitions in voltage-dependent ion channels in terms of transitions from a ferroelectric state to a superionically conducting state, as reviewed by Leuchtag and Bystrov [7]. These theories were motivated by a number of experimental observations in ion channels, including existence of heat-block temperature and thermal hysteresis suggesting possible phase transition, temperature-dependent current suggesting pyroelectricity, surface charges suggesting spontaneous polarization, swelling in response to voltage change suggesting piezoelectricity, as well current-voltage hysteresis and voltage-dependent birefringence that is common in ferroelectrics. It is also interesting to note that a relation between ferroelectricity, liquid crystals and nervous and muscular impulses was predicted by von Hippel [7]. Nevertheless, no direct experimental evidence has been presented.

The indication of ferroelectricity in biological tissue was first reported by Li and Zeng in green abalone shell using piezoresponse force microscopy (PFM) [8], despite earlier probes by a number of leading PFM groups on collagens producing no evidence of switching. Shortly after, working with Yanhang Zhang’s group at Boston University, we observed biological ferroelectricity in aortic wall [9], and almost simultaneously, ferroelectricity was reported in gamma-glycine as well, the smallest amino acid commonly found in protein [10].  We subsequently showed that ferroelectricity in arotic originates from elastin [11], consistent with earlier observations that collagen is not switchable. It is quite interesting to note that collagen is a much more ancient protein than elastin, which is only found in arteries of vertebrate and in later stage of embryonic development, when blood pressure become much higher. This suggests that ferroelectric switching may play a role in damping increased pulsatile flow and blood pressure [12]. In addition, pyroelectricity has long been thought to play a fundamental role in the processes of morphogenesis, which correlates well with observations that elastin is a molecular determinant of late arterial morphogenesis. Furthermore, it is discovered that ferroelectric switching in elastin is largely suppressed by glucose, and this could be related to aging, during which glycation between elastin and sugar naturally occurs.

Despite these progresses, many questions remain. What is the molecular mechanism of biological ferroelectricity, what are possible physiological and pathological implications, and can we take advantage of the phenomena in bio-electronics interfaces? All of these are highly speculative at the moment. In fact, since ferroelectricity has only been demonstrated through PFM so far [13], plenty of doubts remain [14]. More experimental evidences and theoretical understanding are absolutely necessary before the phenomenon is universally accepted. Meanwhile, it is interesting to note that a closely related phenomenon, flexoelectricity, is well established in biology community [15].

We close by arguing that biological ferroelectricity is an exciting frontier demanding interdisciplinary collaborations, and the field will definitely benefit from contributions of ingenious mechanics community. We expect atomic force microscopy will continue to play major role in the exploration, and the readers may be interested in related earlier journal club pieces by Majid Minary (node/11185) and myself (node/10193). On the other hand, we believe exiciting opportunity lies in molecular and quantum mechanics theories, which would shed unprecedented insight into the mechanism of the phenomenon and its implications.

1.         Martin, A. J. P. "Tribo-electricity in wool and hair." Proceedings of the Physical Society 53.2 (1941): 186.

2.         Fukada, Eiichi, and Iwao Yasuda. "On the piezoelectric effect of bone." J. Phys. Soc. Japan 12.10 (1957): 1158-1162. 

3.         Shamos, Morris H. "Piezoelectricity as a fundamental property of biological tissues." Nature 213 (1967): 267-269.

4.         Lang, Sidney B. "Pyroelectric effect in bone and tendon." (1966): 704-705. 

5.         Athenstaedt, Herbert. "Pyroelectric and piezoelectric properties of vertebrates." Annals of the New York Academy of Sciences 238.1 (1974): 68-94.

6.         Lang, Sidney B. "Piezoelectricity, pyroelectricity and ferroelectricity in biomaterials: Speculation on their biological significance." Dielectrics and Electrical Insulation, IEEE Transactions on 7.4 (2000): 466-473. 

7.         Leuchtag, H. Richard, and Vladimir S. Bystrov. "Theoretical models of conformational transitions and ion conduction in voltage-dependent ion channels: Bioferroelectricity and superionic conduction." Ferroelectrics 220.1 (1999): 157-204.

8.         Li, T., and K. Zeng. "Piezoelectric properties and surface potential of green abalone shell studied by scanning probe microscopy techniques." Acta Materialia 59.9 (2011): 3667-3679. 

9.         Liu, Yuanming, et al. "Biological ferroelectricity uncovered in aortic walls by piezoresponse force microscopy." Physical review letters 108.7 (2012): 078103.

10.       Heredia, Alejandro, et al. "Nanoscale Ferroelectricity in Crystalline γ‐Glycine." Advanced Functional Materials 22.14 (2012): 2996-3003. 

11.       Liu, Yuanming, et al. "Glucose suppresses biological ferroelectricity in aortic elastin." Physical review letters 110.16 (2013): 168101.

12.       Chen, Bin, and Huajian Gao. "Are Mammals Ferroelectric?." Physcs Online Journal 5 (2012): 19. 

13.       Kalinin, Sergei V., et al. "Nanoscale electromechanics of ferroelectric and biological systems: a new dimension in scanning probe microscopy." Annu. Rev. Mater. Res. 37 (2007): 189-238.

14.       Scott, J. F. "Prospects for Ferroelectrics: 2012–2022." ISRN Materials Science 2013 (2013). 

15.       Brownell, W. E., et al. "Micro- and nanomechanics of the cochlear outer hair cell." Annual review of biomedical engineering 3.1 (2001): 169-194.

Comments

kyzeng's picture

Thanks Jiangyu to bring this interesting topic. This is an exciting area and definitely needs more work. Following our earlier work [1]. We have continued working in this area in the last two years or so. We have observed the similar behavior in Clamshell [2]. In addition, we applied the flexural stresses to the nacre and then used band-exciation PFM to observed the piezoelectric/ferroelectric properties of the nacre shell [3]. Last year, we presented out work on using Vector PFM and high-voltage PFM on ISAF-PFM 2012 and this work is recently published in the JAP special issue [4]. Hence I believe that the bioferroelectricity is a very unique property and may have a lot of important implications in biological and functional applications of the advanced materials. I agree with Jiangy that this is an exciting frontier research area and AFM is a unique tool for such research activities. Cheers.

Our recent publications in this area:

1. T.Li and K.Zeng, Piezoelectric properties and surface potential of green abalone shell studied by scanning probe microscopy techniques, Acta Mater., 59 (2011), 3667-3679.

2. T.Li and K.Zeng, Nano-hierarchical structure and electromechanical coupling properties of clamshell, J. Struc. Biology, 180 (2012), 73-83.

3. T.Li, L.Chen and K.Zeng, In situ studies of nanoscale electromechanical behavior of nacre under flexural stresses using band excitation PFM, Acta Biomater., 9 (2013), 5903-5912.

4. T.Li and K.Zeng, Nanoscale piezoelectric and ferroelectric behaviors of seashell by piezoresponse force microscopy, J. Appl. Phys., 113, (2013), 187202.

jiangyuli's picture

Kaiyang, thanks for these papers. I assume the switching most occurs in biopolymer regions? To me, the most interesting part is that bone shows no switching behavior while shells do. While their inorganic constituent is similar, the organic compoents appear to be different. Bone possesses mostly collagen, while shells possess elastic biopolymers such as chitin, which I assume is closer to elastin? The molecular structure of chitin also appears to be simple enough for computation?

 Ferroelectric materials is used to make capacitors with tunable capacitance.

 Ferroelectric capacitors are indeed used to make ferroelectric RAM.

 Ferroelectric tunnel junction (FTJ) is used for giant electroresistance (GER) switching effect.

 

 

 

 

Majid Minary's picture

Thanks Jiangyu for this interesting forum. This is a timely discussion on this topic. 

There has been growing evidence in the literature that piezoelectricity and ferroelectricity play critical role in biological function. We have tried piezoelectric measurement on single collagen fibrils. No switching was observed there. But it seems for other ECM materials there is switching.  

Although there are several active patents on piezoelectric implants in the market, the science is still not clear. I believe we need fundamental studies at molecular level to understand the mechanisms and possible biological functions.   

jiangyuli's picture

Thanks Majid, for the comments. One recent paper I should have included is from Brian J. Rodriguez's group,

Denning, D., Alilat, S., Habelitz, S., Fertala, A.,
& Rodriguez, B. J. (2012). Visualizing molecular polar order in
tissues via electromechanical coupling. Journal of Structural Biology.

 

It shows clear phase contrast in collagen fibrils. This makes me think that the switchability of collagen, the the lack of it, maybe is limited by experimental conditions, rather than some fundamental constraint? I could be wrong here though.

 

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