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New insights into why bone is both strong and supple


Having experienced recently an injury to my arm with breaks in three places, I have a fresh appreciation of the remarkable properties of bone. The focus of this blog is not the healing process, but rather the remarkable strength of bone and its ability to withstand intense impacts. The research work under consideration looked at the molecular structure of bone, which means we look with the perspective of nanotechnology. Like many materials, bone has crystalline regions and amorphous regions. The crystalline components (made up of calcium phosphate platelets) are located within a disordered material (the collagen protein matrix). There is also a significant amount of water within bone, and much of it appears to be structural.

“[U]p to 28% of the water associated with bone mineral is highly organized and very strongly bound to mineral, with water hydrogens of the order of ∼2.3–2.55 angstroms from mineral phosphorus atoms. This finding is in sharp contrast with <15% of such a water population for synthetic nanoscopic, carbonated apatite models of bone mineral, suggesting that bone mineral somehow has an extra capacity for strongly bound water compared with synthetic apatitic models. Moreover, there is significant NMR evidence for two distinct sites for structural water in bone mineral. It is worth noting here that heating at 225 degrees C only removes 63% of the water in hydrated bone; clearly, there is a significant population of water molecules that is very difficult to remove." (p.1)

A further feature needing explanation is that increasing the crystallinity of bone introduces weakness. This is a factor that may be relevant to certain medical conditions that result in weakened bones.

“The lack of crystallinity in bone mineral is important – there are many biomechanical studies that show that the degree of crystallinity of the mineral phase is of critical importance to the strength of the bone tissue, with increases in crystallinity associated with impairment in mechanical function.” (p.2)

This brings us to the hypothesis explored in the research. Bone contains about 2% by weight of citrate, but its role, if any, has been uncertain. A new layered structure for bone has been proposed in which citrate and water form bridges between the mineral platelets.

“Another factor that needs to be taken into account is the presence of citrate in bone. Its presence in bone is an accepted fact, but until 2010, there was no attempt to rationalize its presence within a structural model of bone mineral. In 2010, the association of citrate with bone mineral was shown by NMR, and it was proposed that citrate was bound to the surface of bone mineral particles. Given the very close spacing of the mineral platelets in bone [. . .], there is the distinct possibility that, in fact, citrate binds between the surfaces of mineral platelets, helping perhaps to establish the continuum of platelet structures of which bone mineral is observed to consist. Critically, such a structure has the potential to explain the trapping of extra structured water in bone mineral. With this possibility in mind, we propose here a new model for bone mineral, in which disordered citrate ions bridge between the surfaces of apatitic mineral layers or platelets in hydrated layers sandwiched between the mineral platelets.” (p.2)

We shall pass over most of the technical detail in the paper, which tests the hypothesis using a representative material with the name octacalcium phosphate citrate (OCP-citrate), and demonstrates that the new conceptual model satisfactorily explains observations at odds with previous models. This is from their conclusions:

“We have proposed a new model for bone mineral, in which citrate ions are incorporated into the mineral structure in hydrated layers, binding between mineral platelets in a manner akin to the model compound OCP-citrate. The binding of citrate ions between bone mineral platelets can account for many well-known structural features of bone mineral, such as the presence of significant quantities of both strongly bound structural water and disordered but relatively immobile hydrogen phosphate ions in addition to the expected orthophosphate of pure hydroxyapatite. [. . .] The conformation and/or spatial orientation of citrate in the model mineral structure is disordered, and a similar situation in bone mineral would ensure that the atomic structure around the citrate ions, namely the surfaces of the mineral platelets, is also disordered, which in turn, ensures a gap of disordered (and hydrated) material between mineral platelets and prevents the formation of large single crystals that would be detrimental to bone mechanical properties.” (p.9)

According to Dr Melinda Duer, who led the study:

“This nano-scopic layering of citrate fluid and mineral crystals in bone means that the crystals stay in flat, plate-like shapes that have the facility to slide with respect to each other. Without citrate, all crystals in bone mineral would collapse together, become one big crystal and shatter. It’s this layered structure that’s been missing from our knowledge, and we can now see that without it you’re stuffed.” (Source here)

Bone emerges from this study as a highly engineered material. The constituent elements do not self-assemble to form a strong robust frame. Indeed, without citrate in the right places, there is a tendency to form large, single crystals of mineral with corresponding fragility in the bone. “The degree of incorporation of citrate into bone mineral could be important in explaining the changes to bone mineral crystallinity in metabolic diseases” (p.9). It is not unreasonable to postulate the intelligent design of bone and to proceed with research on this basis. Yet the authors affirm on page 2: “If a feature is important in a biological structure, there is generally a mechanism that has evolved to control it”. Apart from the unwarranted use of teleological language, this invoking of evolution is content-free. The central idea in their affirmation makes perfect sense, however, if the rationale is intelligent design.

Citrate bridges between mineral platelets in bone
Erika Davies, Karin H. Muller, Wai Ching Wong, Chris J. Pickard, David G. Reid, Jeremy N. Skepper, and Melinda J. Duer.
Proceedings of the National Academy of Sciences, 2014 DOI: 10.1073/pnas.1315080111

Abstract: We provide evidence that citrate anions bridge between mineral platelets in bone and hypothesize that their presence acts to maintain separate platelets with disordered regions between them rather than gradual transformations into larger, more ordered blocks of mineral. To assess this hypothesis, we take as a model for a citrate bridging between layers of calcium phosphate mineral a double salt octacalcium phosphate citrate (OCP-citrate). [. . .] The proposed structural model that we deduce from this work for bone mineral is a layered structure with thin apatitic platelets sandwiched between OCP-citrate–like hydrated layers. Such a structure can explain a number of known structural features of bone mineral: the thin, plate-like morphology of mature bone mineral crystals, the presence of significant quantities of strongly bound water molecules, and the relatively high concentration of hydrogen phosphate as well as the maintenance of a disordered region between mineral platelets.

See also:

Shock-absorbing ‘goo’ discovered in bone, ScienceDaily (24 March 2014).

Error correction:
This seems like an exiting exciting time for...
This seems like an exciting time for...
My apologies for the misspelling. :( Dionisio
This seems like an exiting time for serious science research. We haven't seen all yet. The party is just starting, the fun part is still ahead. Let's enjoy it. Let's look forward with much anticipation to reading more reports coming out of research labs, shedding more light on the wonderful biological systems. Check out this thread: https://uncommondesc.wpengine.com/evolution/a-third-way-of-evolution/#comment-503971 Dionisio

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