Uncovering the periosteum for skeletal regeneration: The stem cell that lies beneath

Bone

Volumn 70, Issue , 2015, Pages 10-18

  Roberts, Scott J ^a,b,c   van Gastel, Nick ^b   Carmeliet, Geert ^b   Luyten, Frank P ^a,b  

^a SKELETAL BIOLOGY AND ENGINEERING RESEARCH CENTER   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Bone development; Fracture repair; Periosteum; Stem cells; Tissue engineering

Indexed keywords

BONE DEVELOPMENT; BONE GROWTH; BONE MARROW CELL; BONE REGENERATION; BONE REMODELING; BONE TISSUE; CELL COMPOSITION; CHONDROGENESIS; FRACTURE HEALING; HUMAN; NONHUMAN; OSSIFICATION; PERIOSTEAL STEM CELL; PERIOSTEUM; REGENERATIVE MEDICINE; REVIEW; STEM CELL; TISSUE ENGINEERING; ANIMAL; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; REGENERATION;

ANIMALS; BONE DEVELOPMENT; BONE REGENERATION; HUMANS; PERIOSTEUM; REGENERATION; STEM CELLS; TISSUE ENGINEERING;

EID: 84918592050     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2014.08.007     Document Type: Review

References (105)

1. Duhamel H.L. Sur le développement et la crue des os des animaux. Mem Acad R Sci Paris 1742, 354-370.
2. Ollier L. Traite experimentel et clinique de la regeneration des os et de la production artificielle du tissu osseux 1867, V. Masson, Paris.
3. Allen M.R., Hock J.M., Burr D.B. Periosteum: biology, regulation, and response to osteoporosis therapies. Bone 2004, 35:1003-1012.
4. Chanavaz M. Anatomy and histophysiology of the periosteum: quantification of the periosteal blood supply to the adjacent bone with 85Sr and gamma spectrometry. J Oral Implantol 1995, 21:214-219.
5. Colnot C. Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J Bone Miner Res 2009, 24:274-282.
6. Ozaki A., Tsunoda M., Kinoshita S., Saura R. Role of fracture hematoma and periosteum during fracture healing in rats: interaction of fracture hematoma and the periosteum in the initial step of the healing process. J Orthop Sci 2000, 5:64-70.
7. Long F. Building strong bones: molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol 2012, 13:27-38.
8. Ochareon P., Herring S.W. Cell replication in craniofacial periosteum: appositional vs. resorptive sites. J Anat 2011, 218:285-297.
9. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336.
10. Akiyama H., Chaboissier M.C., Martin J.F., Schedl A., de Crombrugghe B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 2002, 16:2813-2828.
11. Akiyama H., Kim J.E., Nakashima K., Balmes G., Iwai N., Deng J.M., et al. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci U S A 2005, 102:14665-14670.
12. Chung U.I., Schipani E., McMahon A.P., Kronenberg H.M. Indian hedgehog couples chondrogenesis to osteogenesis in endochondral bone development. J Clin Invest 2001, 107:295-304.
13. Ornitz D.M., Marie P.J. FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev 2002, 16:1446-1465.
14. Pathi S., Rutenberg J.B., Johnson R.L., Vortkamp A. Interaction of Ihh and BMP/Noggin signaling during cartilage differentiation. Dev Biol 1999, 209:239-253.
15. Maes C., Kobayashi T., Selig M.K., Torrekens S., Roth S.I., Mackem S., et al. Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell 2010, 19:329-344.
16. Seeman E. Periosteal bone formation - a neglected determinant of bone strength. N Engl J Med 2003, 349:320-323.
17. Orwoll E.S. Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res 2003, 18:949-954.
18. Callewaert F., Sinnesael M., Gielen E., Boonen S., Vanderschueren D. Skeletal sexual dimorphism: relative contribution of sex steroids, GH-IGF1, and mechanical loading. J Endocrinol 2010, 207:127-134.
19. Almeida M., Iyer S., Martin-Millan M., Bartell S.M., Han L., Ambrogini E., et al. Estrogen receptor-alpha signaling in osteoblast progenitors stimulates cortical bone accrual. J Clin Invest 2012, 123:394-404.
20. Ogita M., Rached M.T., Dworakowski E., Bilezikian J.P., Kousteni S. Differentiation and proliferation of periosteal osteoblast progenitors are differentially regulated by estrogens and intermittent parathyroid hormone administration. Endocrinology 2008, 149:5713-5723.
21. Orwoll E.S. Androgens: basic biology and clinical implication. Calcif Tissue Int 2001, 69:185-188.
22. Marsell R., Einhorn T.A. The biology of fracture healing. Injury 2011, 42:551-555.
23. Al-Aql Z.S., Alagl A.S., Graves D.T., Gerstenfeld L.C., Einhorn T.A. Molecular mechanisms controlling bone formation during fracture healing and distraction osteogenesis. J Dent Res 2008, 87:107-118.
24. Barnes G.L., Kostenuik P.J., Gerstenfeld L.C., Einhorn T.A. Growth factor regulation of fracture repair. J Bone Miner Res 1999, 14:1805-1815.
25. Cho T.J., Gerstenfeld L.C., Einhorn T.A. Differential temporal expression of members of the transforming growth factor beta superfamily during murine fracture healing. J Bone Miner Res 2002, 17:513-520.
26. Schmid G.J., Kobayashi C., Sandell L.J., Ornitz D.M. Fibroblast growth factor expression during skeletal fracture healing in mice. Dev Dyn 2009, 238:766-774.
27. Yu Y.Y., Lieu S., Lu C., Miclau T., Marcucio R.S., Colnot C. Immunolocalization of BMPs, BMP antagonists, receptors, and effectors during fracture repair. Bone 2010, 46:841-851.
28. Thompson Z., Miclau T., Hu D., Helms J.A. A model for intramembranous ossification during fracture healing. J Orthop Res 2002, 20:1091-1098.
29. Marsh D.R., Li G. The biology of fracture healing: optimising outcome. Br Med Bull 1999, 55:856-869.
30. Zhang X., Xie C., Lin A.S., Ito H., Awad H., Lieberman J.R., et al. Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering. J Bone Miner Res 2005, 20:2124-2137.
31. van Gastel N., Stegen S., Stockmans I., Moermans K., Schrooten J., Graf D., et al. Expansion of murine periosteal progenitor cells with fibroblast growth factor 2 reveals an intrinsic endochondral ossification program mediated by bone morphogenetic protein 2. Stem Cells 2014, 32:2407-2418.
32. Tsuji K., Cox K., Bandyopadhyay A., Harfe B.D., Tabin C.J., Rosen V. BMP4 is dispensable for skeletogenesis and fracture-healing in the limb. J Bone Joint Surg Am 2008, 90:14-18.
33. Tsuji K., Cox K., Gamer L., Graf D., Economides A., Rosen V. Conditional deletion of BMP7 from the limb skeleton does not affect bone formation or fracture repair. J Orthop Res 2010, 28:384-389.
34. Tsuji K., Bandyopadhyay A., Harfe B.D., Cox K., Kakar S., Gerstenfeld L., et al. BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat Genet 2006, 38:1424-1429.
35. Chappuis V., Gamer L., Cox K., Lowery J.W., Bosshardt D.D., Rosen V. Periosteal BMP2 activity drives bone graft healing. Bone 2012, 51:800-809.
36. Wang Q., Huang C., Xue M., Zhang X. Expression of endogenous BMP-2 in periosteal progenitor cells is essential for bone healing. Bone 2011, 48:524-532.
37. Eyckmans J., Roberts S.J., Schrooten J., Luyten F.P. A clinically relevant model of osteoinduction: a process requiring calcium phosphate and BMP/Wnt signalling. J Cell Mol Med 2010, 14:1845-1856.
38. Behr B., Leucht P., Longaker M.T., Quarto N. Fgf-9 is required for angiogenesis and osteogenesis in long bone repair. Proc Natl Acad Sci U S A 2010, 107:11853-11858.
39. Coutu D.L., Francois M., Galipeau J. Inhibition of cellular senescence by developmentally regulated FGF receptors in mesenchymal stem cells. Blood 2011, 117:6801-6812.
40. Rundle C.H., Miyakoshi N., Ramirez E., Wergedal J.E., Lau K.H., Baylink D.J. Expression of the fibroblast growth factor receptor genes in fracture repair. Clin Orthop Relat Res 2002, 253-263.
41. Du X., Xie Y., Xian C.J., Chen L. Role of FGFs/FGFRs in skeletal development and bone regeneration. J Cell Physiol 2012, 227:3731-3743.
42. Le A.X., Miclau T., Hu D., Helms J.A. Molecular aspects of healing in stabilized and non-stabilized fractures. J Orthop Res 2001, 19:78-84.
43. Murakami S., Noda M. Expression of Indian hedgehog during fracture healing in adult rat femora. Calcif Tissue Int 2000, 66:272-276.
44. Wang Q., Huang C., Zeng F., Xue M., Zhang X. Activation of the Hh pathway in periosteum-derived mesenchymal stem cells induces bone formation in vivo: implication for postnatal bone repair. Am J Pathol 2010, 177:3100-3111.
45. Huang C., Tang M., Yehling E., Zhang X. Overexpressing sonic hedgehog peptide restores periosteal bone formation in a murine bone allograft transplantation model. Mol Ther 2014, 22:430-439.
46. Gerstenfeld L.C., Cho T.J., Kon T., Aizawa T., Tsay A., Fitch J., et al. Impaired fracture healing in the absence of TNF-alpha signaling: the role of TNF-alpha in endochondral cartilage resorption. J Bone Miner Res 2003, 18:1584-1592.
47. Xie C., Ming X., Wang Q., Schwarz E.M., Guldberg R.E., O'Keefe R.J., et al. COX-2 from the injury milieu is critical for the initiation of periosteal progenitor cell mediated bone healing. Bone 2008, 43:1075-1083.
48. Zhang X., Schwarz E.M., Young D.A., Puzas J.E., Rosier R.N., O'Keefe R.J. Cyclooxygenase-2 regulates mesenchymal cell differentiation into the osteoblast lineage and is critically involved in bone repair. J Clin Invest 2002, 109:1405-1415.
49. Hilton M.J., Tu X., Wu X., Bai S., Zhao H., Kobayashi T., et al. Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat Med 2008, 14:306-314.
50. Matthews B.G., Grcevic D., Wang L., Hagiwara Y., Roguljic H., Joshi P., et al. Analysis of αSMA-labeled progenitor cell commitment identifies notch signaling as an important pathway in fracture healing. J Bone Miner Res 2014, 29:1283-1294.
51. Komatsu D.E., Mary M.N., Schroeder R.J., Robling A.G., Turner C.H., Warden S.J. Modulation of Wnt signaling influences fracture repair. J Orthop Res 2010, 28:928-936.
52. Minear S., Leucht P., Jiang J., Liu B., Zeng A., Fuerer C., et al. Wnt proteins promote bone regeneration. Sci Transl Med 2010, 2:29-30.
53. Baron R., Kneissel M. WNT signaling in bone homeostasis and disease: from human mutations to treatments. Nat Med 2013, 19:179-192.
54. Chang H., Knothe Tate M.L. Concise review: the periosteum: tapping into a reservoir of clinically useful progenitor cells. Stem Cells Transl Med 2012, 1:480-491.
55. Arnsdorf E.J., Jones L.M., Carter D.R., Jacobs C.R. The periosteum as a cellular source for functional tissue engineering. Tissue Eng Part A 2009, 15:2637-2642.
56. Breitbart A.S., Grande D.A., Kessler R., Ryaby J.T., Fitzsimmons R.J., Grant R.T. Tissue engineered bone repair of calvarial defects using cultured periosteal cells. Plast Reconstr Surg 1998, 101:567-574.
57. Declercq H.A., De Ridder L.I., Cornelissen M.J. Isolation and osteogenic differentiation of rat periosteum-derived cells. Cytotechnology 2005, 49:39-50.
58. Eyckmans J., Luyten F.P. Species specificity of ectopic bone formation using periosteum-derived mesenchymal progenitor cells. Tissue Eng 2006, 12:2203-2213.
59. Nakahara H., Bruder S.P., Goldberg V.M., Caplan A.I. In vivo osteochondrogenic potential of cultured cells derived from the periosteum. Clin Orthop Relat Res 1990, 259:223-232.
60. van Gastel N., Torrekens S., Roberts S.J., Moermans K., Schrooten J., Carmeliet P., et al. Engineering vascularized bone: osteogenic and proangiogenic potential of murine periosteal cells. Stem Cells 2012, 30:2460-2471.
61. De Bari C., Dell'Accio F., Vanlauwe J., Eyckmans J., Khan I.M., Archer C.W., et al. Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. Arthritis Rheum 2006, 54:1209-1221.
62. Roberts S.J., Owen H.C., Tam W.L., Solie L., Van Cromphaut S.J., Van den Berghe G., et al. Humanized culture of periosteal progenitors in allogeneic serum enhances osteogenic differentiation and in vivo bone formation. Stem Cells Transl Med 2014, 3:218-228.
63. Nakahara H., Dennis J.E., Bruder S.P., Haynesworth S.E., Lennon D.P., Caplan A.I. In vitro differentiation of bone and hypertrophic cartilage from periosteal-derived cells. Exp Cell Res 1991, 195:492-503.
64. Roberts S.J., Geris L., Kerckhofs G., Desmet E., Schrooten J., Luyten F.P. The combined bone forming capacity of human periosteal derived cells and calcium phosphates. Biomaterials 2011, 32:4393-4405.
65. Bianco P., Cao X., Frenette P.S., Mao J.J., Robey P.G., Simmons P.J., et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat Med 2013, 19:35-42.
66. Lim S.M., Choi Y.S., Shin H.C., Lee C.W., Kim D.I. Isolation of human periosteum-derived progenitor cells using immunophenotypes for chondrogenesis. Biotechnol Lett 2005, 27:607-611.
67. Stich S., Loch A., Leinhase I., Neumann K., Kaps C., Sittinger M., 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.
68. Eyckmans J., Roberts S.J., Bolander J., Schrooten J., Chen C.S., Luyten F.P. Mapping calcium phosphate activated gene networks as a strategy for targeted osteoinduction of human progenitors. Biomaterials 2013, 34:4612-4621.
69. Roberts S.J., Chen Y., Moesen M., Schrooten J., Luyten F.P. Enhancement of osteogenic gene expression for the differentiation of human periosteal derived cells. Stem Cell Res 2011, 7:137-144.
70. Chai Y.C., Roberts S.J., Schrooten J., Luyten F.P. Probing the osteoinductive effect of calcium phosphate by using an in vitro biomimetic model. Tissue Eng Part A 2011, 17:1083-1097.
71. Chai Y.C., Roberts S.J., Desmet E., Kerckhofs G., van Gastel N., Geris L., et al. Mechanisms of ectopic bone formation by human osteoprogenitor cells on CaP biomaterial carriers. Biomaterials 2012, 33:3127-3142.
72. Grcevic D., Pejda S., Matthews B.G., Repic D., Wang L., Li H., et al. In vivo fate mapping identifies mesenchymal progenitor cells. Stem Cells 2012, 30:187-196.
73. Kawanami A., Matsushita T., Chan Y.Y., Murakami S. Mice expressing GFP and CreER in osteochondro progenitor cells in the periosteum. Biochem Biophys Res Commun 2009, 386:477-482.
74. Murao H., Yamamoto K., Matsuda S., Akiyama H. Periosteal cells are a major source of soft callus in bone fracture. J Bone Miner Metab 2013, 31:390-398.
75. Mendez-Ferrer S., Michurina T.V., Ferraro F., Mazloom A.R., Macarthur B.D., Lira S.A., et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010, 466:829-834.
76. Park D., Spencer J.A., Koh B.I., Kobayashi T., Fujisaki J., Clemens T.L., et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 2012, 10:259-272.
77. Sacchetti B., Funari A., Michienzi S., Di Cesare S., Piersanti S., Saggio I., et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007, 131:324-336.
78. Diaz-Flores L., Gutierrez R., Lopez-Alonso A., Gonzalez R., Varela H. Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis. Clin Orthop Relat Res 1992, 280-286.
79. Simpson A.H. The blood supply of the periosteum. J Anat 1985, 140:697-704.
80. Nakahara H., Goldberg V.M., Caplan A.I. Culture-expanded human periosteal-derived cells exhibit osteochondral potential in vivo. J Orthop Res 1991, 9:465-476.
81. Bakker A.D., Schrooten J., van Cleynenbreugel T., Vanlauwe J., Luyten J., Schepers E., et al. Quantitative screening of engineered implants in a long bone defect model in rabbits. Tissue Eng Part C Methods 2008, 14:251-260.
82. Perka C., Schultz O., Spitzer R.S., Lindenhayn K., Burmester G.R., Sittinger M. Segmental bone repair by tissue-engineered periosteal cell transplants with bioresorbable fleece and fibrin scaffolds in rabbits. Biomaterials 2000, 21:1145-1153.
83. Redlich A., Perka C., Schultz O., Spitzer R., Haupl T., Burmester G.R., et al. Bone engineering on the basis of periosteal cells cultured in polymer fleeces. J Mater Sci Mater Med 1999, 10:767-772.
84. Sakata Y., Ueno T., Kagawa T., Kanou M., Fujii T., Yamachika E., et al. Osteogenic potential of cultured human periosteum-derived cells - a pilot study of human cell transplantation into a rat calvarial defect model. J Craniomaxillofac Surg 2006, 34:461-465.
85. Srouji S., Ben-David D., Funari A., Riminucci M., Bianco P. Evaluation of the osteoconductive potential of bone substitutes embedded with schneiderian membrane- or maxillary bone marrow-derived osteoprogenitor cells. Clin Oral Implants Res 2013, 24:1288-1294.
86. Agata H., Asahina I., Yamazaki Y., Uchida M., Shinohara Y., Honda M.J., et al. Effective bone engineering with periosteum-derived cells. J Dent Res 2007, 86:79-83.
87. Vacanti C.A., Bonassar L.J., Vacanti M.P., Shufflebarger J. Replacement of an avulsed phalanx with tissue-engineered bone. N Engl J Med 2001, 344:1511-1514.
88. Schimming R., Schmelzeisen R. Tissue-engineered bone for maxillary sinus augmentation. J Oral Maxillofac Surg 2004, 62:724-729.
89. Schmelzeisen R., Schimming R., Sittinger M. Making bone: implant insertion into tissue-engineered bone for maxillary sinus floor augmentation - a preliminary report. J Craniomaxillofac Surg 2003, 31:34-39.
90. Springer I.N., Nocini P.F., Schlegel K.A., De S.D., Park J., Warnke P.H., et al. Two techniques for the preparation of cell-scaffold constructs suitable for sinus augmentation: steps into clinical application. Tissue Eng 2006, 12:2649-2656.
91. Hayashi O., Katsube Y., Hirose M., Ohgushi H., Ito H. Comparison of osteogenic ability of rat mesenchymal stem cells from bone marrow, periosteum, and adipose tissue. Calcif Tissue Int 2008, 82:238-247.
92. Sakaguchi Y., Sekiya I., Yagishita K., Muneta T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 2005, 52:2521-2529.
93. Radtke C.L., Nino-Fong R., Esparza Gonzalez B.P., Stryhn H., McDuffee L.A. Characterization and osteogenic potential of equine muscle tissue- and periosteal tissue-derived mesenchymal stem cells in comparison with bone marrow- and adipose tissue-derived mesenchymal stem cells. Am J Vet Res 2013, 74:790-800.
94. Yoshimura H., Muneta T., Nimura A., Yokoyama A., Koga H., Sekiya I. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res 2007, 327:449-462.
95. Dominici M., Le B.K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
96. Stockmann P., Park J., von Wilmowsky C., Nkenke E., Felszeghy E., Dehner J.F., 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.
97. Pelissier P., Martin D., Baudet J., Lepreux S., Masquelet A.C. Behaviour of cancellous bone graft placed in induced membranes. Br J Plast Surg 2002, 55:596-598.
98. Pelissier P., Masquelet A.C., Bareille R., Pelissier S.M., Amedee J. Induced membranes secrete growth factors including vascular and osteoinductive factors and could stimulate bone regeneration. J Orthop Res 2004, 22:73-79.
99. Cuthbert R.J., Churchman S.M., Tan H.B., McGonagle D., Jones E., Giannoudis P.V. Induced periosteum a complex cellular scaffold for the treatment of large bone defects. Bone 2013, 57:484-492.
100. Catros S., Zwetyenga N., Bareille R., Brouillaud B., Renard M., Amedee J., et al. Subcutaneous-induced membranes have no osteoinductive effect on macroporous HA-TCP in vivo. J Orthop Res 2009, 27:155-161.
101. Hoffman M.D., Benoit D.S. Emerging ideas: engineering the periosteum: revitalizing allografts by mimicking autograft healing. Clin Orthop Relat Res 2013, 471:721-726.
102. Schonmeyr B., Clavin N., Avraham T., Longo V., Mehrara B.J. Synthesis of a tissue-engineered periosteum with acellular dermal matrix and cultured mesenchymal stem cells. Tissue Eng Part A 2009, 15:1833-1841.
103. Xie C., Reynolds D., Awad H., Rubery P.T., Pelled G., Gazit D., et al. Structural bone allograft combined with genetically engineered mesenchymal stem cells as a novel platform for bone tissue engineering. Tissue Eng 2007, 13:435-445.
104. Long T., Zhu Z., Awad H.A., Schwarz E.M., Hilton M.J., Dong Y. The effect of mesenchymal stem cell sheets on structural allograft healing of critical sized femoral defects in mice. Biomaterials 2014, 35:2752-2759.
105. Chang C.H., Chen C.H., Liu H.W., Whu S.W., Chen S.H., Tsai C.L., et al. Bioengineered periosteal progenitor cell sheets to enhance tendon-bone healing in a bone tunnel. Biomed J 2012, 35:473-480.