Periosteal Sharpey's fibers: a novel bone matrix regulatory system?

Abstract

Sharpey's "perforating" fibers (SF) are well known skeletally in tooth anchorage. Elsewhere they provide anchorage for the periosteum and are less well documented. Immunohistochemistry has transformed their potential significance by identifying their collagen type III (CIII) content and enabling their mapping in domains as permeating arrays of fibers (5-25 μ thick), protected from osteoclastic resorption by their poor mineralization. As periosteal extensions they are crucial in early skeletal development and central to intramembranous bone healing, providing unique microanatomical avenues for musculoskeletal exchange, their composition (e.g., collagen type VI, elastin, tenascin) combined with a multiaxial pattern of insertion suggesting a role more complex than attachment alone would justify. A proportion permeate the cortex to the endosteum (and beyond), fusing into a CIII-rich osteoid layer (<2 μ thick) encompassing all resting surfaces, and with which they apparently integrate into a PERIOSTEAL-SHARPEY FIBER-ENDOSTEUM (PSE) structural continuum. This intraosseous system behaves in favor of bone loss or gain depending upon extraneous stimuli (i.e., like Frost's hypothetical "mechanostat"). Thus, the birefringent fibers are sensitive to humoral factors (e.g., estrogen causes retraction, rat femur model), physical activity (e.g., running causes expansion, rat model), aging (e.g., causes fragmentation, pig mandible model), and pathology (e.g., atrophied in osteoporosis, hypertrophied in osteoarthritis, human proximal femur), and with encroaching mineral particles hardening the usually soft parts. In this way the unobtrusive periosteal SF network may regulate bone status, perhaps even contributing to predictable "hotspots" of trabecular disconnection, particularly at sites of tension prone to fatigue, and with the network deteriorating significantly before bone matrix loss.

Keywords: collagen type III; collagen type VI; elastin; endosteal membrane; matrix biochemical domains; skeletal aging; tenascin.

FIGURE 1

Photomicrograph of a typical representative array of three periosteal Sharpey’s fibers (black arrows), each about 15 μm thick, and extending from the periosteum (P), through the bone (B) toward the endosteum outside which is the marrow cavity (MC). In addition, nearby are stress-induced microcracks, for example, one (white arrow) is surrounded by bone matrix which has become “leaky” to the stain (normally impervious) apparently due to submicroscopic fatigue fissures increasing accessibility of the dye. Human proximal femur. En bloc gentian violet stain. Scale bar 30 μm.

FIGURE 2

Photomicrograph of two typical representative collagen type III-rich Sharpey’s fibers, about 10 μm thick, and fluorescing positive within the negative calcified bone matrix. Human proximal femur. FITC-immunostain for CIII, UV epifluorescence microscopy. Scale bar 10 μm. After Carter et al. (1992).

FIGURE 3

Diagram showing (A) a stylized CIII/CVI-rich periosteal Sharpey’s fiber with adherent beaded chains of tenascin and encircled by a coil of elastin, and (B) tracings of the same coarse fibers (about 15 μm diameter) in cross section showing their typical irregular profiles. After Aaron and Skerry (1994).

FIGURE 4

Diagram of a mature rat femur showing the gross configuration of the expansive CIII/CVI-rich proximal domain of Sharpey fiber bone (striped area), terminating in CII/CVI-rich “anchors” (round dots), (A) in a normal control, (B) expanded in response to voluntary running exercise, and (C) contracted in response to OVX. After Luther et al. (2003) and Saino et al. (2003).

FIGURE 5

Diagram illustrating the conductance of a hypothetical stimulus to the periosteal membrane (P) across the adjacent CIII-rich Sharpey fiber domain to its direct interface with the inner domain where the act is translated into a reaction of increased vascularity via osteopontin (OPN)-rich new haversian systems.

FIGURE 6

Diagram of the postulated periosteal-Sharpey’s fiber-endosteal (PSE) integrated system. (A) In youth when it is multiaxial and pervasive with oblique insertions predominant and with a well defined CIII-rich endosteal rim. (B) With age and osteoporosis when insertions are more polarized horizontally, with general signs of regression and fragmentation, and with a discontinuous CIII-rich endosteal rim; also associated are sparsely distributed fine mineral microparticles, about 1 μm diameter, that may alter flexibility. (C) In osteoarthritis, similarly characterized by more numerous horizontal insertions and a more heterogeneous incidence of prominent thickened fibers, and with a CIII-rich endosteal rim that is widened in places; also associated are frequent coarse mineral microparticles, about 2 μm diameter, that may increase stiffness. After Al-Qtaitat (2007) and Al-Qtaitat et al. (2010)).