Elucidating Multiscale Periosteal Mechanobiology: a Key to Unlocking the Smart Properties and Regenerative Capacity of the Periosteum?

Overview

Journal Tissue Eng Part B Rev

Specialties Anatomy & Histology
Biotechnology

Date 2012 Nov 30

PMID 23189933

Citations 38

Authors

Sarah F Evans

Hana Chang

Melissa L Knothe Tate

Affiliations

Soon will be listed here.

Abstract

The periosteum, a thin, fibrous tissue layer covering most bones, resides in a dynamic, mechanically loaded environment. The periosteum also provides a niche for mesenchymal stem cells. The mechanics of periosteum vary greatly between species and anatomical locations, indicating the specialized role of periosteum as bone's bounding membrane. Furthermore, periosteum exhibits stress-state-dependent mechanical and material properties, hallmarks of a smart material. This review discusses what is known about the multiscale mechanical and material properties of the periosteum as well as their potential effect on the mechanosensitive progenitor cells within the tissue. Furthermore, this review addresses open questions and barriers to understanding periosteum's multiscale structure-function relationships. Knowledge of the smart material properties of the periosteum will maximize the translation of periosteum and substitute periosteum to regenerative medicine, facilitate the development of biomimetic tissue-engineered periosteum for use in instances where the native periosteum is lacking or damaged, and provide inspiration for a new class of smart, advanced materials.

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References

Bishop G, Einhorn T . Current and future clinical applications of bone morphogenetic proteins in orthopaedic trauma surgery. Int Orthop. 2007; 31(6):721-7. PMC: 2266667. DOI: 10.1007/s00264-007-0424-8. View

Isaksson H, Comas O, van Donkelaar C, Mediavilla J, Wilson W, Huiskes R . Bone regeneration during distraction osteogenesis: mechano-regulation by shear strain and fluid velocity. J Biomech. 2006; 40(9):2002-11. DOI: 10.1016/j.jbiomech.2006.09.028. View

HSIEH Y, Turner C . Effects of loading frequency on mechanically induced bone formation. J Bone Miner Res. 2001; 16(5):918-24. DOI: 10.1359/jbmr.2001.16.5.918. View

Solchaga L, Cassiede P, Caplan A . Different response to osteo-inductive agents in bone marrow- and periosteum-derived cell preparations. Acta Orthop Scand. 1998; 69(4):426-32. DOI: 10.3109/17453679808999061. View

Moukoko D, Pourquier D, Pithioux M, Chabrand P . Influence of cyclic bending loading on in vivo skeletal tissue regeneration from periosteal origin. Orthop Traumatol Surg Res. 2010; 96(8):833-9. DOI: 10.1016/j.otsr.2010.07.006. View

Saris D, Sanyal A, An K, Fitzsimmons J, ODriscoll S . Periosteum responds to dynamic fluid pressure by proliferating in vitro. J Orthop Res. 1999; 17(5):668-77. DOI: 10.1002/jor.1100170508. View

Ribeiro F, Suaid F, Ruiz K, Rodrigues T, Carvalho M, Nociti F . Peri-implant reconstruction using autologous periosteum-derived cells and guided bone regeneration. J Clin Periodontol. 2010; 37(12):1128-36. DOI: 10.1111/j.1600-051X.2010.01635.x. View

Reichert J, Cipitria A, Epari D, Saifzadeh S, Krishnakanth P, Berner A . A tissue engineering solution for segmental defect regeneration in load-bearing long bones. Sci Transl Med. 2012; 4(141):141ra93. DOI: 10.1126/scitranslmed.3003720. View

Discher D, Janmey P, Wang Y . Tissue cells feel and respond to the stiffness of their substrate. Science. 2005; 310(5751):1139-43. DOI: 10.1126/science.1116995. View

10.

Yamamiya K, Okuda K, Kawase T, Hata K, Wolff L, Yoshie H . Tissue-engineered cultured periosteum used with platelet-rich plasma and hydroxyapatite in treating human osseous defects. J Periodontol. 2008; 79(5):811-8. DOI: 10.1902/jop.2008.070518. View

11.

Bertram J, Polevoy Y, Cullinane D . Mechanics of avian fibrous periosteum: tensile and adhesion properties during growth. Bone. 1998; 22(6):669-75. DOI: 10.1016/s8756-3282(98)00035-0. View

12.

Vidyadhara S, Rao S . A novel approach to juxta-articular aggressive and recurrent giant cell tumours: resection arthrodesis using bone transport over an intramedullary nail. Int Orthop. 2006; 31(2):179-84. PMC: 2267554. DOI: 10.1007/s00264-006-0150-7. View

13.

Al-Qtaitat A, Shore R, Aaron J . Structural changes in the ageing periosteum using collagen III immuno-staining and chromium labelling as indicators. J Musculoskelet Neuronal Interact. 2010; 10(1):112-23. View

14.

Kubo K, Att W, Yamada M, Ohmi K, Tsukimura N, Suzuki T . Microtopography of titanium suppresses osteoblastic differentiation but enhances chondroblastic differentiation of rat femoral periosteum-derived cells. J Biomed Mater Res A. 2008; 87(2):380-91. DOI: 10.1002/jbm.a.31791. View

15.

Arnsdorf E, Jones L, Carter D, Jacobs C . The periosteum as a cellular source for functional tissue engineering. Tissue Eng Part A. 2009; 15(9):2637-42. PMC: 2792114. DOI: 10.1089/ten.TEA.2008.0244. View

16.

Kanno T, Takahashi T, Ariyoshi W, Tsujisawa T, Haga M, Nishihara T . Tensile mechanical strain up-regulates Runx2 and osteogenic factor expression in human periosteal cells: implications for distraction osteogenesis. J Oral Maxillofac Surg. 2005; 63(4):499-504. DOI: 10.1016/j.joms.2004.07.023. View

17.

Knothe Tate M, Dolejs S, McBride S, Miller R, Knothe U . Multiscale mechanobiology of de novo bone generation, remodeling and adaptation of autograft in a common ovine femur model. J Mech Behav Biomed Mater. 2011; 4(6):829-40. PMC: 3742371. DOI: 10.1016/j.jmbbm.2011.03.009. View

18.

Li M, Amizuka N, Oda K, Tokunaga K, Ito T, Takeuchi K . Histochemical evidence of the initial chondrogenesis and osteogenesis in the periosteum of a rib fractured model: implications of osteocyte involvement in periosteal chondrogenesis. Microsc Res Tech. 2004; 64(4):330-42. DOI: 10.1002/jemt.20088. View

19.

McBride S, Knothe Tate M . Modulation of stem cell shape and fate A: the role of density and seeding protocol on nucleus shape and gene expression. Tissue Eng Part A. 2008; 14(9):1561-72. DOI: 10.1089/ten.tea.2008.0112. View

20.

Mara C, Sartori A, Duarte A, Andrade A, Pedro M, Coimbra I . Periosteum as a source of mesenchymal stem cells: the effects of TGF-β3 on chondrogenesis. Clinics (Sao Paulo). 2011; 66(3):487-92. PMC: 3072013. DOI: 10.1590/s1807-59322011000300022. View