Translating Periosteum's Regenerative Power: Insights From Quantitative Analysis of Tissue Genesis With a Periosteum Substitute Implant

Moore, Shannon R.; Heu, Céline; Yu, Na; Whan, Renée; Knothe, Ulf; Milz, Stefan; Tate, Melissa L. Knothe

doi:10.5966/sctm.2016-0004

Cited by 31 publications

(33 citation statements)

References 73 publications

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“…The rationale for the choice of the ovine model was twofold. First, we aimed to build on our previous body of work using the ovine model and its translation from in vitro , , to ex vivo to in vivo , , , to clinical studies , , . Also, in contrast to the few cell layer‐thick murine periosteum , the ovine femoral periosteal thickness approximates that of humans , .…”

Section: Methodsmentioning

confidence: 99%

“…The periosteum, a composite cellular and connective tissue, bounds all nonarticular bone surfaces and provides a niche for mesenchymal stem cells (MSCs) . Hyperelastic periosteal tissue exhibits a remarkable regenerative capacity; in critical size long bone defects surrounded in situ by periosteum, periosteum‐derived cells (PDCs) egress from the tissue sheath within days of injury to regenerate tissue, infilling the defect with intramembranous woven bone within weeks or endochondrally produced bone within months . This process is modulated by both PDCs and periosteum's endogenous extracellular matrix (ECM) proteins , .…”

Section: Introductionmentioning

confidence: 99%

“…Hyperelastic periosteal tissue exhibits a remarkable regenerative capacity; in critical size long bone defects surrounded in situ by periosteum, periosteum‐derived cells (PDCs) egress from the tissue sheath within days of injury to regenerate tissue, infilling the defect with intramembranous woven bone within weeks or endochondrally produced bone within months . This process is modulated by both PDCs and periosteum's endogenous extracellular matrix (ECM) proteins , . Mechanical loading has been shown to correlate with an increase in periosteum's tissue regeneration capacity , .…”

Section: Introductionmentioning

confidence: 99%

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Live Tissue Imaging to Elucidate Mechanical Modulation of Stem Cell Niche Quiescence

O'Brien

Šlapetová

et al. 2016

Stem Cells Translational Medicine

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The periosteum, a composite cellular connective tissue, bounds all nonarticular bone surfaces. Like Velcro, collagenous Sharpey's fibers anchor the periosteum in a prestressed state to the underlying bone. The periosteum provides a niche for mesenchymal stem cells. Periosteal lifting, as well as injury, causes cells residing in the periosteum (PDCs) to change from an immobile, quiescent state to a mobile, active state. The physical cues that activate PDCs to home to and heal injured areas remain a conundrum. An understanding of these cues is key to unlocking periosteum's remarkable regenerative power. We hypothesized that changes in periosteum's baseline stress state modulate the quiescence of its stem cell niche. We report, for the first time, a three‐dimensional, high‐resolution live tissue imaging protocol to observe and characterize ovine PDCs and their niche before and after release of the tissue's endogenous prestress. Loss of prestress results in abrupt shrinkage of the periosteal tissue. At the microscopic scale, loss of prestress results in significantly increased crimping of collagen of periosteum's fibrous layer and a threefold increase in the number of rounded nuclei in the cambium layer. Given the body of published data describing the relationships between stem cell and nucleus shape, structure and function, these observations are consistent with a role for mechanics in the modulation of periosteal niche quiescence. The quantitative characterization of periosteum as a stem cell niche represents a critical step for clinical translation of the periosteum and periosteum substitute‐based implants for tissue defect healing. Stem Cells Translational Medicine 2017;6:285–292

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Live Tissue Imaging to Elucidate Mechanical Modulation of Stem Cell Niche Quiescence

O'Brien

Šlapetová

et al. 2016

Stem Cells Translational Medicine

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“…In the outer most layer of the periosteum, collagens and elastin provide fibrous structure that assists in regulating the flow of molecules between bone and muscle. 71,72 The inner most layer consists of the progenitor cells that contribute to bone homeostasis and fracture repair. The cellular response to fracture within the periosteum is observed as early as 24–48 hours post-injury through rapid proliferation.…”

Section: Stem Cell Contribution To Fracture Repairmentioning

confidence: 99%

Origin of Reparative Stem Cells in Fracture Healing

Bragdon

Bahney

2018

Curr Osteoporos Rep

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Functional studies show MSCs are not the multipotential stem cell population that form cartilage and bone during fracture repair. Rather, multiple studies have confirmed the periosteum is the primary source of stem/progenitor cells for fracture repair. Newer work is also identifying other stem/progenitor cells that may also contribute to healing. Although the heterogenous periosteal cells migrate to the fracture site and contribute directly to callus formation, other cell populations are involved. Pericytes and bone marrow stromal cells are now thought of as key secretory centers that mostly coordinate the repair process. Other populations of stem/progenitor cells from the muscle and transdifferentiated chondroctyes may also contribute to repair, and their functional role is an area of active research.

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“…The periosteum serves as an interface between bone and muscles and thus as a gatekeeper for transfer of molecular and physical (stresses, strains) information between the two tissue compartments1314. Like Velcro, collagen containing Sharpey’s fibers anchor periosteum to bone, serving as a link between the external musculature and the internal skeleton115.…”

mentioning

confidence: 99%

Scale-up of nature’s tissue weaving algorithms to engineer advanced functional materials

Knothe

Whan

et al. 2017

Sci Rep

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We are literally the stuff from which our tissue fabrics and their fibers are woven and spun. The arrangement of collagen, elastin and other structural proteins in space and time embodies our tissues and organs with amazing resilience and multifunctional smart properties. For example, the periosteum, a soft tissue sleeve that envelops all nonarticular bony surfaces of the body, comprises an inherently “smart” material that gives hard bones added strength under high impact loads. Yet a paucity of scalable bottom-up approaches stymies the harnessing of smart tissues’ biological, mechanical and organizational detail to create advanced functional materials. Here, a novel approach is established to scale up the multidimensional fiber patterns of natural soft tissue weaves for rapid prototyping of advanced functional materials. First second harmonic generation and two-photon excitation microscopy is used to map the microscopic three-dimensional (3D) alignment, composition and distribution of the collagen and elastin fibers of periosteum, the soft tissue sheath bounding all nonarticular bone surfaces in our bodies. Then, using engineering rendering software to scale up this natural tissue fabric, as well as multidimensional weaving algorithms, macroscopic tissue prototypes are created using a computer-controlled jacquard loom. The capacity to prototype scaled up architectures of natural fabrics provides a new avenue to create advanced functional materials.

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Translating Periosteum's Regenerative Power: Insights From Quantitative Analysis of Tissue Genesis With a Periosteum Substitute Implant

Abstract: This study used an interdisciplinary, quantitative approach to assess tissue genesis in modular periosteum substitute implants, with the aim to provide translational strategies for regenerative medicine and tissue engineering.

Cited by 31 publications

References 73 publications

Live Tissue Imaging to Elucidate Mechanical Modulation of Stem Cell Niche Quiescence

Live Tissue Imaging to Elucidate Mechanical Modulation of Stem Cell Niche Quiescence

Origin of Reparative Stem Cells in Fracture Healing

Scale-up of nature’s tissue weaving algorithms to engineer advanced functional materials

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