Concise review: The periosteum: Tapping into a reservoir of clinically useful progenitor cells

Stem Cells Translational Medicine

Volumn 1, Issue 6, 2012, Pages 480-491

  Chang, Hana ^a   Tate, Melissa L Knothe ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Bone marrow stromal cells; Clinical translation; Stem progenitor cell; Tissue regeneration; Tissue specific stem cells

Indexed keywords

ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; ALKALINE PHOSPHATASE; CD14 ANTIGEN; CD9 ANTIGEN; COLLAGEN; DEXAMETHASONE; ENDOGLIN; ESTROGEN; PARATHYROID HORMONE; PROTEIN SH2; PROTEIN SH3; THY 1 ANTIGEN;

APOPTOSIS; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; EXTRACELLULAR MATRIX; FRACTURE HEALING; HUMAN; MESENCHYMAL STEM CELL; MICRO-COMPUTED TOMOGRAPHY; MORPHOLOGY; MULTIPOTENT STEM CELL; NONHUMAN; OSTEOBLAST; PERIOSTEUM; PHENOTYPE; REGENERATIVE ABILITY; REVIEW; STEM CELL; STEM CELL NICHE; TISSUE REGENERATION; TRANSLATIONAL RESEARCH; UMBILICAL CORD BLOOD;

EID: 84867850102     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2011-0056     Document Type: Review

References (139)

1. Duhamel HL. Sur le Developpement et la Crue des os des animaux. Mem Acad Roy Des Sci 1742;55:354-357.
2. Ollier L. Recherches experimentales sur les greffes osseuses. J Physiol Homme Animaux 1860;3:88.
3. Ueno T, Kagawa T, Mizukawa N et al. Cellular origin of endochondral ossification from grafted periosteum. Anat Rec 2001;264:348-357.
4. Young RW. Cell proliferation and specialization during endochondral osteogenesis in young rats. J Cell Biol 1962;14:357-370.
5. Yu YY, Lieu S, Lu C et al. Bone morphogenetic protein 2 stimulates endochondral ossification by regulating periosteal cell fate during bone repair. Bone 2010;47:65-73.
6. Shapiro F. Bone development and its relation to fracture repair. The role of mesenchymal osteoblasts and surface osteoblasts. Eur Cell Mater 2008;15:53-76.
7. Arnsdorf EJ, Jones LM, Carter DR et al. The periosteum as a cellular source for functional tissue engineering. Tissue Eng Part A 2009;15: 2637-2642.
8. Puelacher WC, Vacanti JP, Ferraro NF et al. Femoral shaft reconstruction using tissue-engineered growth of bone. Int J Oral Maxillofac Surg 1996;25:223-228.
9. Knothe UR, Springfield DS. A novel surgical procedure for bridging of massive bone defects. World J Surg Oncol 2005;3:7.
10. Knothe Tate ML, Ritzman TF, Schneider E et al. Testing of a new one-stage bone-transport surgical procedure exploiting the periosteum for the repair of long-bone defects. J Bone Joint Surg Am 2007;89:307-316.
11. Putzier M, Strube P, Funk J et al. Periosteal cells compared with autologous cancellous bone in lumbar segmental fusion. J Neurosurg Spine 2008;8:536-543.
12. Karaoglu S, Celik C, Korkusuz P. The effects of bone marrow or periosteum on tendon-tobone tunnel healing in a rabbit model. Knee Surg Sports Traumatol Arthrosc 2009;17:170-178.
13. Thabet AM, Paley D, Kocaoglu M et al. Periosteal grafting for congenital pseudarthrosis of the tibia: A preliminary report. Clin Orthop Relat Res 2008;466:2981-2994.
14. Mahajan A. Periosteum: A highly underrated tool in dentistry. Int J Dent 2012;2012: 717-816.
15. Stockmann P, Park J, von Wilmowsky C et al. Guided bone regeneration in pig calvarial bone defects using autologous mesenchymal stem/progenitor cells: A comparison of different tissue sources. J Craniomaxillofac Surg 2012;40:310-320.
16. Keskin M, Kelly CP, Moreira-Gonzalez A et al. Repairing critical-sized rat calvarial defects with a periosteal cell-seeded small intestinal submucosal layer. Plast Reconstr Surg 2008;122:400-409.
17. Squier CA, Ghoneim S, Kremenak CR. Ultrastructure of the periosteum from membrane bone. J Anat 1990;171:233-239.
18. McBride SH, Evans SF, Knothe Tate ML. Anisotropic mechanical properties of ovine femoral periosteum and the effects of cryopreservation. J Biomech 2011;44:1954-1959.
19. Ochareon P, Herring SW. Growing the mandible: Role of the periosteum and its cells. Anat Rec (Hoboken) 2007;290:1366-1376.
20. Foolen J, van Donkelaar C, Nowlan N et al. Collagen orientation in periosteum and perichondrium is aligned with preferential directions of tissue growth. J Orthop Res 2008; 26:1263-1268.
21. Lim SM, Choi YS, Shin HC et al. Isolation of human periosteum-derived progenitor cells using immunophenotypes for chondrogenesis. Biotechnol Lett 2005;27:607-611.
22. Stich S, Loch A, Leinhase I et al. Human periosteum-derived progenitor cells express distinct chemokine receptors and migrate upon stimulation with CCL2, CCL25, CXCL8, CXCL12, and CXCL13. Eur J Cell Biol 2008;87:365-376.
23. Choi YS, Noh SE, Lim SM et al. Multipotency and growth characteristic of periosteumderived progenitor cells for chondrogenic, osteogenic, and adipogenic differentiation. Biotechnol Lett 2008;30:593-601.
24. Allen MR, Hock JM, Burr DB. Periosteum: Biology, regulation, and response to osteoporosis therapies. Bone 2004;35:1003-1012.
25. Dwek JR. The periosteum: What is it, where is it, and what mimics it in its absence? Skeletal Radiol 2010;39:319-323.
26. Brighton CT, Lorich DG, Kupcha R et al. The pericyte as a possible osteoblast progenitor cell. Clin Orthop Relat Res 1992;275:287-299.
27. Diaz-Flores L, Gutierrez R, Gonzalez P et al. Inducible perivascular cells contribute to the neochondrogenesis in grafted perichondrium. Anat Rec 1991;229:1-8.
28. Diaz-Flores L, Gutierrez R, Lopez-Alonso A et al. Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis. Clin Orthop Relat Res 1992;275:280-286.
29. Bae S, Ahn JH, Park CW et al. Gene and microRNA expression signatures of human mesenchymal stromal cells in comparison to fibroblasts. Cell Tissue Res 2009;335:565-573.
30. Chen FG, Zhang WJ, Bi D et al. Clonal analysis of nestin() vimentin() multipotent fibroblasts isolated from human dermis. J Cell Sci 2007;120:2875-2883.
31. Feldon SE, O'Loughlin CW, Ray DM et al. Activated human T lymphocytes express cyclooxygenase-2 and produce proadipogenic prostaglandins that drive human orbital fibroblast differentiation to adipocytes. Am J Pathol 2006;169:1183-1193.
32. Haniffa MA, Collin MP, Buckley CD et al. Mesenchymal stem cells: The fibroblasts' new clothes? Haematologica 2009;94:258-263.
33. Lorenz K, Sicker M, Schmelzer E et al. Multilineage differentiation potential of human dermal skin-derived fibroblasts. Exp Dermatol 2008;17:925-932.
34. Lysy PA, Smets F, Sibille C et al. Human skin fibroblasts: From mesodermal to hepatocyte-like differentiation. Hepatology 2007;46: 1574-1585.
35. Bassi EJ, Aita CAM, Câmara NOS. Immune regulatory properties of multipotent mesenchymal stromal cells: Where do we stand? World J Stem Cells 2011;3:1-8.
36. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007;110:3499-3506.
37. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315-317.
38. Jones E, McGonagle D. Human bone marrow mesenchymal stem cells in vivo. Rheumatology 2008;47:126-131.
39. Morikawa S, Mabuchi Y, Kubota Y et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med 2009;206:2483-2496.
40. Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: Revisiting history, concepts, and assays. Cell Stem Cell 2008;2:313-319.
41. Wolf CB, Mohammad RK. Mechanotransduction and Its Role in Stem Cell Biology. In: Baharvand H, ed. Trends in Stem Cell Biology and Technology. Totowa, NJ: Humana Press, 2009:389-403.
42. Augello A, Kurth TB, De Bari C. Mesenchymal stem cells: A perspective from in vitro cultures to in vivo migration and niches. Eur Cell Mater 2010;20:121-133.
43. Mara CS, Sartori AR, Duarte AS et al. Periosteum as a source of mesenchymal stem cells: The effects of TGF-3 on chondrogenesis. Clinics (Sao Paulo) 2011;66:487-492.
44. Ma D, Yao H, Tian W et al. Enhancing bone formation by transplantation of a scaffold-free tissue-engineered periosteum in a rabbit model. Clin Oral Implants Res 2011;22: 1193-1199.
45. Agata H, Asahina I, Yamazaki Y et al. Effective bone engineering with periosteum-derived cells. J Dent Res 2007;86:79-83.
46. Ribeiro FV, Suaid FF, Ruiz KGS et al. Periosteum-derived cells as an alternative to bone marrow cells for bone tissue engineering around dental implants. A histomorphometric study in beagle dogs. J Periodontol 2010;81:907-916.
47. Hayashi O, Katsube Y, Hirose M et al. Comparison of osteogenic ability of rat mesenchymal stem cells from bone marrow, periosteum, and adipose tissue. Calcif Tissue Int 2008;82:238-247.
48. Mafi R, Hindocha S, Mafi P et al. Sources of adult mesenchymal stem cells applicable for musculoskeletal applications: A systematic review of the literature. Open Orthop J 2011;5: 242-248.
49. Knothe Tate ML, Chang H, Moore SR et al. Surgical membranes as directional delivery devices to generate tissue: Testing in an ovine critical sized defect model. PLoS One 2011;6:e28702.
50. Knothe Tate ML, Yu M, Knothe U. Regeneration of periosteum in denuded bone. Trans Orthop Res Soc 2011;36:1453.
51. Mercurio AD, Motta T, Green E et al. Effects of extensive circumferential periosteal stripping on the microstructure and mechanical properties of the murine femoral cortex. J Orthop Res 2012;30:561-568.
52. da Vieira Silva R, Camilli JA. Periosteal donor site regeneration in rats. J Submicrosc Cytol Pathol 2002;34:187-190.
53. Merritt FJW, Erinc AM, Knothe Tate ML. Periosteum regenerates on periosteum-denuded, transported bone segment. Trans Orthop Res Soc 2012;37:1570.
54. Moore S, Knothe U, Knothe Tate ML. Elucidation of cellular mechanisms underlying efficacy of a periosteal replacement membrane. Trans Orthop Res Soc 2011;36:1454.
55. Bruder SP, Jaiswal N, Haynesworth SE. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem 1997;64:278-294.
56. Koshihara Y, Honda Y. Age-related increase in collagen production in cultured human osteoblast-like periosteal cells. Mech Ageing Dev 1994;74:89-101.
57. Tornberg DN, Bassett CA. Activation of the resting periosteum. Clin Orthop Relat Res 1977:305-312.
58. De Bari C, Dell'Accio F, Luyten FP. Human periosteum-derived cells maintain phenotypic stability and chondrogenic potential throughout expansion regardless of donor age. Arthritis Rheum 2001;44:85-95.
59. De Bari C, Dell'Accio F, Vanlauwe J et al. Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. Arthritis Rheum 2006;54:1209-1221.
60. McBride SH, Dolejs S, Brianza S et al. Net change in periosteal strain during stance shift loading after surgery correlates to rapid de novo bone generation in critically sized defects. Ann Biomed Eng 2011;39:1570-1581.
61. Bilkay U, Tokat C, Helvaci E et al. Osteogenic capacities of tibial and cranial periosteum: A biochemical and histologic study. J Craniofac Surg 2008;19:453-458.
62. Fan W, Crawford R, Xiao Y. Structural and cellular differences between metaphyseal and diaphyseal periosteum in different aged rats. Bone 2008;42:81-89.
63. Gallay SH, Miura Y, Commisso CN et al. Relationship of donor site to chondrogenic potential of periosteum in vitro. J Orthop Res 1994;12:515-525.
64. Srisa-Art M, Bonzani IC, Williams A et al. Identification of rare progenitor cells from human periosteal tissue using droplet microfluidics. Analyst 2009;134:2239-2245.
65. Ogita M, Rached MT, Dworakowski E et al. Differentiation and proliferation of periosteal osteoblast progenitors are differentially regulated by estrogens and intermittent parathyroid hormone administration. Endocrinology 2008;149:5713-5723.
66. Alexander D, Schäfer F, Munz A et al. LNGFR induction during osteogenesis of human jaw periosteum-derived cells. Cell Physiol Biochem 2009;24:283-290.
67. Ballock RT, Heydemann A, Izumi T et al. Regulation of the expression of the type-II collagen gene in periosteum-derived cells by three members of the transforming growth factor-beta superfamily. J Orthop Res 1997;15: 463-467.
68. Ochareon P, Herring SW. Growing the mandible: Role of the periosteum and its cells. Anat Rec (Hoboken) 2007;290:1366-1376.
69. Declercq HA, De Ridder LI, Cornelissen MJ. Isolation and osteogenic differentiation of rat periosteum-derived cells. Cytotechnology 2005;49:39-50.
70. Demol J, Eyckmans J, Roberts SJ et al. Does tranexamic acid stabilised fibrin support the osteogenic differentiation of human periosteum derived cells? Eur Cell Mater 2011;21:272-285.
71. Eyckmans J, Luyten FP. Species specificity of ectopic bone formation using periosteum-derived mesenchymal progenitor cells. Tissue Eng 2006;12:2203-2213.
72. Izumi T, Scully SP, Heydemann A et al. Transforming growth factor beta 1 stimulates type II collagen expression in cultured periosteum-derived cells. J Bone Miner Res 1992;7: 115-121.
73. Jones DB, Nolte H, Scholübbers JG et al. Biochemical signal transduction of mechanical strain in osteoblast-like cells. Biomaterials 1991;12:101-110.
74. Kubo K, Att W, Yamada M et al. Microtopography of titanium suppresses osteoblastic differentiation but enhances chondroblastic differentiation of rat femoral periosteum-derived cells. J Biomed Mater Res A 2008;87:380-391.
75. Nakata K, Nakahara H, Kimura T et al. Collagen gene expression during chondrogenesis from chick periosteum-derived cells. FEBS Lett 1992;299:278-282.
76. Nakase T, Nakahara H, Iwasaki M et al. Clonal analysis for developmental potential of chick periosteum-derived cells: Agar gel culture system. Biochem Biophys Res Commun 1993;195:1422-1428.
77. Park J, Gelse K, Frank S et al. Transgeneactivated mesenchymal cells for articular cartilage repair: A comparison of primary bone marrow-, perichondrium/periosteumand fatderived cells. J Gene Med 2006;8:112-125.
78. Roberts SJ, Chen Y, Moesen M et al. Enhancement of osteogenic gene expression for the differentiation of human periosteal derived cells. Stem Cell Res 2011;7:137-144.
79. Solchaga LA, Cassiède P, Caplan AI. Different response to osteo-inductive agents in bone marrowand periosteum-derived cell preparations. Acta Orthop Scand 1998;69:426-432.
80. Wu X, Lin M, Li Y et al. Effects of DMEM and RPMI 1640 on the biological behavior of dog periosteum-derived cells. Cytotechnology 2009;59:103-111.
81. Brownlow HC, Reed A, Joyner C et al. Anatomical effects of periosteal elevation. J Orthop Res 2000;18:500-502.
82. Sakai D, Kii I, Nakagawa K et al. Remodeling of actin cytoskeleton in mouse periosteal cells under mechanical loading induces periosteal cell proliferation during bone formation. PLoS One 2011;6:e24847.
83. Hutmacher DW, Sittinger M. Periosteal cells in bone tissue engineering. Tissue Eng 2003;9:S45-S64.
84. Choi YS, Lim SM, Shin HC et al. Chondrogenesis of human periosteum-derived progenitor cells in atelocollagen. Biotechnol Lett 2007;29:323-329.
85. Samee M, Kasugai S, Kondo H et al. Bone morphogenetic protein-2 (BMP-2) and vascular endothelial growth factor (VEGF) transfection to human periosteal cells enhances osteoblast differentiation and bone formation. J Pharmacol Sci 2008;108: 18-31.
86. Castro-Silva II, Zambuzzi WF, de Oliveira Castro L et al. Periosteal-derived cells for bone bioengineering: A promising candidate. Clin Oral Implants Res 2012 (in press).
87. Ball MD, Bonzani IC, Bovis MJ et al. Human periosteum is a source of cells for orthopaedic tissue engineering: A pilot study. Clin Orthop Relat Res 2011;469:3085-3093.
88. Yoshimura H, Muneta T, Nimura A et al. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res 2007;327:449-462.
89. Nakahara H, Watanabe K, Sugrue SP et al. Temporal and spatial distribution of type XII collagen in high cell density culture of periosteal-derived cells. Dev Biol 1990;142:481-485.
90. Nakahara H, Dennis JE, Bruder SP et al. In vitro differentiation of bone and hypertrophic cartilage from periosteal-derived cells. Exp Cell Res 1991;195:492-503.
91. O'Driscoll SW, Saris DB, Ito Y et al. The chondrogenic potential of periosteum decreases with age. J Orthop Res 2001;19:95-103.
92. Justesen J, Stenderup K, Eriksen EF et al. Maintenance of osteoblastic and adipocytic differentiation potential with age and osteoporosis in human marrow stromal cell cultures. Calcif Tissue Int 2002;71:36-44.
93. Stenderup K, Justesen J, Clausen C et al. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003;33:919-926.
94. Stolzing A, Jones E, McGonagle D et al. Age-related changes in human bone marrowderived mesenchymal stem cells: Consequences for cell therapies. Mech Ageing Dev 2008;129:163-173.
95. Zhang W, Ou G, Hamrick M et al. Agerelated changes in the osteogenic differentiation potential of mouse bone marrow stromal cells. J Bone Miner Res 2008;23:1118-1128.
96. Bellantuono I, Aldahmash A, Kassem M. Aging of marrow stromal (skeletal) stem cells and their contribution to age-related bone loss. Biochim Biophys Acta 2009;1792:364-370.
97. Zou L, Zou X, Chen L et al. Multilineage differentiation of porcine bone marrow stromal cells associated with specific gene expression pattern. J Orthop Res 2008;26:56-64.
98. Jaiswal N, Haynesworth SE, Caplan AI et al. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 1997;64:295-312.
99. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284: 143-147.
100. Li Q, Tang J, Wang R et al. Comparing the chondrogenic potential in vivo of autogeneic mesenchymal stem cells derived from different tissues. Artif Cells Blood Substit Immobil Biotechnol 2011;39:31-38.
101. Knothe Tate ML, Falls TD, McBride SH et al. Mechanical modulation of osteochondroprogenitor cell fate. Int J Biochem Cell Biol 2008;40:2720-2738.
102. Anderson EA, Knothe Tate ML. Design of tissue engineering scaffolds as delivery devices for mechanical and mechanically modulated signals. Tissue Eng 2007;13: 2525-2538.
103. McBride SH, Knothe Tate ML. Modulation of stem cell shape and fate A: Role of density and seeding protocol on nucleus shape and gene expression. Tissue Eng 2008;14:1561-1572.
104. McBride SH, Falls T, Knothe Tate ML. Modulation of stem cell shape and fate B: Mechanical modulation of cell shape and gene expression. Tissue Eng Part A 2008;14:1573-1580.
105. Zimmermann JA, Knothe Tate ML. Structure-function relationships in the stem cell's mechanical world A: Seeding protocols as a means to control shape and fate of live stem cells. Mol Cell Biomech 2011;8:275-296.
106. Chang H, Knothe Tate ML. Structurefunction relationships in the stem cell's mechanical world B: Emergent anisotropy of the cytoskeleton correlates to volume and shape changing stress exposure. Mol Cell Biomech 2011;8:297-318.
107. Knothe Tate ML. Top down and bottom up engineering of bone. J Biomech 2011;44: 304-312.
108. Jang JY, Lee SW, Park SH et al. Combined effects of surface morphology and mechanical straining magnitudes on the differentiation of mesenchymal stem cells without using biochemical reagents. J Biomed Biotechnol 2011;2011:860652.
109. Tonna EA, Cronkite EP. The effects of extraperiosteal injections of blood components on periosteal cell proliferation. J Cell Biol 1964;23:79-87.
110. Knothe UR, Dolejs S, Miller MR et al. Effects of mechanical loading patterns, bone graft, and proximity to periosteum on bone defect healing. J Biomech 2010;43:2728-2737.
111. Pead MJ, Skerry TM, Lanyon LE. Direct transformation from quiescence to bone formation in the adult periosteum following a single brief period of bone loading. J Bone Miner Res 1988;3:647-656.
112. Raab-Cullen DM, Thiede MA, Petersen DN et al. Mechanical loading stimulates rapid changes in periosteal gene expression. Calcif Tissue Int 1994;55:473-478.
113. Simon TM, Van Sickle DC, Kunishima DH et al. Cambium cell stimulation from surgical release of the periosteum. J Orthop Res 2003; 21:470-480.
114. Thomson RC, Mikos AG, Beahm E et al. Guided tissue fabrication from periosteum using preformed biodegradable polymer scaffolds. Biomaterials 1999;20:2007-2018.
115. Saris DB, Sanyal A, An KN et al. Periosteum responds to dynamic fluid pressure by proliferating in vitro. J Orthop Res 1999;17: 668-677.
116. Mukherjee N, Saris DB, Schultz FM et al. The enhancement of periosteal chondrogenesis in organ culture by dynamic fluid pressure. J Orthop Res 2001;19:524-530.
117. Miller RM, McBride SH, Dolejs S et al. Modeling the mechanobiology of the periosteum to predict and harness its regenerative capacity. Trans Orthop Res Soc 2011;36: 2213.
118. Kearney CJ, Lee JY, Padera RF et al. Extracorporeal shock wave-induced proliferation of periosteal cells. J Orthop Res 2011;29:1536-1543.
119. Ryu YM, Hah YS, Park BW et al. Osteogenic differentiation of human periostealderived cells in a three-dimensional collagen scaffold. Mol Biol Rep 2011;38:2887-2894.
120. Takeuchi K, Saruwatari L, Nakamura HK et al. Enhanced intrinsic biomechanical properties of osteoblastic mineralized tissue on roughened titanium surface. J Biomed Mater Res A 2005;72:296-305.
121. Sorkin AM, Dee KC, Knothe Tate ML. "Culture shock" from the bone cell's perspective: Emulating physiological conditions for mechanobiological investigations. Am J Physiol Cell Physiol 2004;287:C1527-C1536.
122. Anderson EJ, Falls TD, Sorkin A et al. The imperative for controlled mechanical stresses in unraveling cellular mechanisms of mechanotransduction. Biomed Eng Online 2006;5:27.
123. Anderson EJ, Knothe Tate ML. Open access to novel flow chamber technology for in vitro cell mechanotransduction, toxicity and pharmacokinetic studies. Biomed Eng Online 2007;6:46.
124. Breitbart AS, Grande DA, Kessler R et al. Tissue engineered bone repair of calvarial defects using cultured periosteal cells. Plast Reconstr Surg 1998;101:567-574.
125. Isogai N, Landis WJ, Mori R et al. Experimental use of fibrin glue to induce sitedirected osteogenesis from cultured periosteal cells. Plast Reconstr Surg 2000;105: 953-963.
126. Jaquiéry C, Schaeren S, Farhadi J et al. In vitro osteogenic differentiation and in vivo bone-forming capacity of human isogenic jaw periosteal cells and bone marrow stromal cells. Ann Surg 2005;242:859-867.
127. Ono T, Yoshida T, Hoh C et al. A morphological study on the response between primary periosteum cultures and synthetic hydroxyapatite particles. Shika Kiso Igakkai Zasshi 1990;32:83-86.
128. Perka C, Schultz O, Spitzer RS et al. Segmental bone repair by tissue-engineered periosteal cell transplants with bioresorbable fleece and fibrin scaffolds in rabbits. Biomaterials 2000;21:1145-1153.
129. Redlich A, Perka C, Schultz O et al. Bone engineering on the basis of periosteal cells cultured in polymer fleeces. J Mater Sci Mater Med 1999;10:767-772.
130. Wakitani S, Goto T, Pineda SJ et al. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am 1994;76:579-592.
131. Shimizu T, Sasano Y, Nakajo S et al. Osteoblastic differentiation of periosteum-derived cells is promoted by the physical contact with the bone matrix in vivo. Anat Rec 2001; 264:72-81.
132. Hah YS, Jun JS, Lee SG et al. Vascular endothelial growth factor stimulates osteoblastic differentiation of cultured human periosteal-derived cells expressing vascular endothelial growth factor receptors. Mol Biol Rep 2011;38:1443-1450.
133. Song MJ, Dean D, Brady-Kalnay S et al. Optimization of tissue engineering scaffold geometry, seeding and flow conditions to steer stem cell shape and fate. TERMIS (Tissue Engineering Regenerative Medicine International Society) North America, Houston, TX. December 11-14, 2011.
134. Rubinstein P. Cord blood banking for clinical transplantation. Bone Marrow Transplant 2009;44:635-642.
135. Bieback K, Brinkmann I. Mesenchymal stromal cells from human perinatal tissues: From biology to cell therapy. World J Stem Cells 2010;2:81-92.
136. Cherubino P, Ratti C, Fagetti A et al. Total hip arthroplasty and bone fragility. Aging Clin Exp Res 2011;23(suppl):76-77.
137. Evans SF, Parent J, Knothe Tate ML. Permeability properties of ovine femoral periosteum. Trans Orthop Res Soc 2012;37:1355.
138. Zhang X, Awad HA, O'Keefe RJ et al. A perspective: Engineering periosteum for structural bone graft healing. Clin Orthop Relat Res 2008;466:1777-1787.
139. Colnot C. Cell sources for bone tissue engineering: Insights from basic science. Tissue Eng Part B Rev 2011;17:449-457.