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Review Article | Open Access

Signaling pathways in osteogenesis and osteoclastogenesis: Lessons from cranial sutures and applications to regenerative medicine

Justin B. Maxhimera, James P. Bradleyb, Justine C. Leea,c( )
Division of Plastic and Reconstructive Surgery, UCLA David Geffen School of Medicine, CA, USA
Division of Plastic and Reconstructive Surgery, Temple University/St. Christopher’s Hospital for Children, PA, USA
Division of Plastic and Reconstructive Surgery, Greater Los Angeles VA Healthcare System, USA

Peer review under responsibility of Chongqing Medical University.

Show Author Information

Abstract

One of the simplest models for examining the interplay between bone formation and resorption is the junction between the cranial bones. Although only roughly a quarter of patients diagnosed with craniosynostosis have been linked to known genetic disturbances, the molecular mechanisms elucidated from these studies have provided basic knowledge of bone homeostasis. This work has translated to methods and advances in bone tissue engineering. In this review, we examine the current knowledge of cranial suture biology derived from human craniosynostosis syndromes and discuss its application to regenerative medicine.

Keywords

Tissue engineeringSignalingOsteogenesisOsteoclastCraniosynostosisOPGRANKRANKL

References

1

Bradley JP, Levine JP, Blewett C, Krummel T, McCarthy JG, Longaker MT. Studies in cranial suture biology: in vitro cranial suture fusion. Cleft Palate Craniofac J. 1996;33:150–156.
Crossref Google Scholar
2
Bradley JP, Levine JP, McCarthy JG, Longaker MT. Studies in cranial suture biology: regional dura mater determines in vitro cranial suture fusion. Plast Reconstr Surg. 1997;100: 1091–1099. discussion; 1100–1092.
Crossref
3

Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM. Tissue origins and interactions in the mammalian skull vault. Dev Biol. 2002;241:106–116.
Crossref Google Scholar
4

Yoshida T, Vivatbutsiri P, Morriss-Kay G, Saga Y, Iseki S. Cell lineage in mammalian craniofacial mesenchyme. Mech Dev. 2008;125:797–808.
Crossref Google Scholar
5

Singer S, Bower C, Southall P, Goldblatt J. Craniosynostosis in Western Australia, 1980–1994: a population-based study. Am J Med Genet. 1999;83:382–387.
Crossref Google Scholar
6

Boulet SL, Rasmussen SA, Honein MA. A population-based study of craniosynostosis in metropolitan Atlanta, 1989–2003. Am J Med Genet A. 2008;146A:984–991.
Crossref Google Scholar
7

Lajeunie E, Le Merrer M, Bonaiti-Pellie C, Marchac D, Renier D. Genetic study of nonsyndromic coronal craniosynostosis. Am J Med Genet. 1995;55:500–504.
Crossref Google Scholar
8

Renier D, Sainte-Rose C, Marchac D, Hirsch JF. Intracranial pressure in craniostenosis. J Neurosurg. 1982;57:370–377.
Crossref Google Scholar
9

Maliepaard M, Mathijssen IM, Oosterlaan J, Okkerse JM. Intellectual, behavioral, and emotional functioning in children with syndromic craniosynostosis. Pediatrics. 2014;133:e1608–e1615.
Crossref Google Scholar
10

Hashim PW, Patel A, Yang JF, et al. The effects of whole-vault cranioplasty versus strip craniectomy on long-term neuropsychological outcomes in sagittal craniosynostosis. Plast Reconstr Surg. 2014;134:491–501.
Crossref Google Scholar
11

Patel A, Yang JF, Hashim PW, et al. The impact of age at surgery on long-term neuropsychological outcomes in sagittal craniosynostosis. Plast Reconstr Surg. 2014;134:e608–e617.
Crossref Google Scholar
12

Bradley JP, Lee JC. Discussion: the effects of whole-vault cranioplasty versus strip craniectomy on long-term neuropsychological outcomes in sagittal craniosynostosis. Plast Reconstr Surg. 2014;134:502–503.
Crossref Google Scholar
13

Wilkie AO. Craniosynostosis: genes and mechanisms. Hum Mol Genet. 1997;6:1647–1656.
Crossref Google Scholar
14

Sharma VP, Fenwick AL, Brockop MS, et al. Mutations in TCF12, encoding a basic helix-loop-helix partner of TWIST1, are a frequent cause of coronal craniosynostosis. Nat Genet. 2013;45:304–307.
Crossref Google Scholar
15

Twigg SR, Vorgia E, McGowan SJ, et al. Reduced dosage of ERF causes complex craniosynostosis in humans and mice and links ERK1/2 signaling to regulation of osteogenesis. Nat Genet. 2013;45:308–313.
Crossref Google Scholar
16

Fitzpatrick DR. Filling in the gaps in cranial suture biology. Nat Genet. 2013;45:231–232.
Crossref Google Scholar
17

Muenke M, Gripp KW, McDonald-McGinn DM, et al. A unique point mutation in the fibroblast growth factor receptor 3 gene (FGFR3) defines a new craniosynostosis syndrome. Am J Hum Genet. 1997;60:555–564.
Google Scholar
18

Ma L, Golden S, Wu L, Maxson R. The molecular basis of Boston-type craniosynostosis: the Pro148->His mutation in the N-terminal arm of the MSX2 homeodomain stabilizes DNA binding without altering nucleotide sequence preferences. Hum Mol Genet. 1996;5:1915–1920.
Crossref Google Scholar
19

Robinson IB, Sarnat BG. Growth pattern of the pig mandible; a serial roentgenographic study using metallic implants. Am J Anat. 1955;96:37–64.
Crossref Google Scholar
20

Parfitt AM. Targeted and nontargeted bone remodeling: relationship to basic multicellular unit origination and progression. Bone. 2002;30:5–7.
Crossref Google Scholar
21

Bar-Shavit Z. The osteoclast: a multinucleated, hematopoietic-origin, bone-resorbing osteoimmune cell. J Cell Biochem. 2007;102:1130–1139.
Crossref Google Scholar
22

Robling AG, Castillo AB, Turner CH. Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng. 2006;8:455–498.
Crossref Google Scholar
23

Castro-Malaspina H, Gay RE, Resnick G, et al. Characterization of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny. Blood. 1980;56:289–301.
Crossref Google Scholar
24

Hedgecock NL, Hadi T, Chen AA, Curtiss SB, Martin RB, Hazelwood SJ. Quantitative regional associations between remodeling, modeling, and osteocyte apoptosis and density in rabbit tibial midshafts. Bone. 2007;40:627–637.
Crossref Google Scholar
25

Burger EH, Klein-Nulend J. Mechanotransduction in bone–role of the lacuno-canalicular network. FASEB J. 1999;(suppl 13):S101–S112.
Crossref Google Scholar
26

Reardon W, Winter RM, Rutland P, Pulleyn LJ, Jones BM, Malcolm S. Mutations in the fibroblast growth factor receptor 2 gene cause Crouzon syndrome. Nat Genet. 1994;8:98–103.
Crossref Google Scholar
27

Sagong B, Jung d J, Baek JI, et al. Identification of causative mutation in a Korean family with Crouzon syndrome using whole exome sequencing. Ann Clin Lab Sci. 2014;44:476–483.
Google Scholar
28

Meyers GA, Orlow SJ, Munro IR, Przylepa KA, Jabs EW. Fibroblast growth factor receptor 3 (FGFR3) transmembrane mutation in Crouzon syndrome with acanthosis nigricans. Nat Genet. 1995;11:462–464.
Crossref Google Scholar
29

Keupp K, Li Y, Vargel I, et al. Mutations in the interleukin receptor IL11RA cause autosomal recessive Crouzon-like craniosynostosis. Mol Genet Genomic Med. 2013;1:223–237.
Crossref Google Scholar
30

Nieminen P, Morgan NV, Fenwick AL, et al. Inactivation of IL11 signaling causes craniosynostosis, delayed tooth eruption, and supernumerary teeth. Am J Hum Genet. 2011;89:67–81.
Crossref Google Scholar
31

Yeh E, Fanganiello RD, Sunaga DY, et al. Novel molecular pathways elicited by mutant FGFR2 may account for brain abnormalities in Apert syndrome. PLoS One. 2013;8:e60439.
Crossref Google Scholar
32

el Ghouzzi V, Le Merrer M, Perrin-Schmitt F, et al. Mutations of the TWIST gene in the Saethre-Chotzen syndrome. Nat Genet. 1997;15:42–46.
Crossref Google Scholar
33

Howard TD, Paznekas WA, Green ED, et al. Mutations in TWIST, a basic helix-loop-helix transcription factor, in Saethre-Chotzen syndrome. Nat Genet. 1997;15:36–41.
Crossref Google Scholar
34

Lajeunie E, Ma HW, Bonaventure J, Munnich A, Le Merrer M, Renier D. FGFR2 mutations in Pfeiffer syndrome. Nat Genet. 1995;9:108.
Crossref Google Scholar
35

Muenke M, Schell U, Hehr A, et al. A common mutation in the fibroblast growth factor receptor 1 gene in Pfeiffer syndrome. Nat Genet. 1994;8:269–274.
Crossref Google Scholar
36

Jabs EW, Müller U, Li X, et al. A mutation in the homeodomain of the human MSX2 gene in a family affected with autosomal dominant craniosynostosis. Cell. 1993;75:443–450.
Crossref Google Scholar
37

Przylepa KA, Paznekas W, Zhang M, et al. Fibroblast growth factor receptor 2 mutations in Beare-Stevenson cutis gyrata syndrome. Nat Genet. 1996;13:492–494.
Crossref Google Scholar
38

Wieland I, Jakubiczka S, Muschke P, et al. Mutations of the ephrin-B1 gene cause craniofrontonasal syndrome. Am J Hum Genet. 2004;74:1209–1215.
Crossref Google Scholar
39

Jabs EW, Li X, Scott AF, et al. Jackson-Weiss and Crouzon syndromes are allelic with mutations in fibroblast growth factor receptor 2. Nat Genet. 1994;8:275–279.
Crossref Google Scholar
40

Lattanzi W, Bukvic N, Barba M, et al. Genetic basis of single-suture synostoses: genes, chromosomes and clinical implications. Childs Nerv Syst. 2012;28:1301–1310.
Crossref Google Scholar
41

Eswarakumar VP, Lax I, Schlessinger J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 2005;16:139–149.
Crossref Google Scholar
42

Wilkie AO, Slaney SF, Oldridge M, et al. Apert syndrome results from localized mutations of FGFR2 and is allelic with Crouzon syndrome. Nat Genet. 1995;9:165–172.
Crossref Google Scholar
43

Liu YH, Tang Z, Kundu RK, et al. Msx2 gene dosage influences the number of proliferative osteogenic cells in growth centers of the developing murine skull: a possible mechanism for MSX2-mediated craniosynostosis in humans. Dev Biol. 1999;205:260–274.
Crossref Google Scholar
44

Spector JA, Mathy JA, Warren SM, et al. FGF-2 acts through an ERK1/2 intracellular pathway to affect osteoblast differentiation. Plast Reconstr Surg. 2005;115:838–852.
Crossref Google Scholar
45

Dodig M, Tadic T, Kronenberg MS, et al. Ectopic Msx2 overexpression inhibits and Msx2 antisense stimulates calvarial osteoblast differentiation. Dev Biol. 1999;209:298–307.
Crossref Google Scholar
46

Bruderer M, Richards RG, Alini M, Stoddart MJ. Role and regulation of RUNX2 in osteogenesis. Eur Cell Mater. 2014;28:269–286.
Crossref Google Scholar
47

Greives MR, Odessey EA, Waggoner DJ, et al. RUNX2 quadruplication: additional evidence toward a new form of syndromic craniosynostosis. J Craniofac Surg. 2013;24:126–129.
Crossref Google Scholar
48

Ducy P, Karsenty G. The family of bone morphogenetic proteins. Kidney Int. 2000;57:2207–2214.
Crossref Google Scholar
49

Mueller TD, Nickel J. Promiscuity and specificity in BMP receptor activation. FEBS Lett. 2012;586:1846–1859.
Crossref Google Scholar
50

Miyazono K, Kamiya Y, Morikawa M. Bone morphogenetic protein receptors and signal transduction. J Biochem. 2010;147:35–51.
Crossref Google Scholar
51

Koenig BB, Cook JS, Wolsing DH, et al. Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol Cell Biol. 1994;14:5961–5974.
Crossref Google Scholar
52

Townson SA, Martinez-Hackert E, Greppi C, et al. Specificity and structure of a high affinity activin receptor-like kinase 1 (ALK1) signaling complex. J Biol Chem. 2012;287:27313–27325.
Crossref Google Scholar
53

Nohe A, Hassel S, Ehrlich M, et al. The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J Biol Chem. 2002;277:5330–5338.
Crossref Google Scholar
54

Gilboa L, Nohe A, Geissendörfer T, Sebald W, Henis YI, Knaus P. Bone morphogenetic protein receptor complexes on the surface of live cells: a new oligomerization mode for serine/threonine kinase receptors. Mol Biol Cell. 2000;11:1023–1035.
Crossref Google Scholar
55

Lou J, Tu Y, Li S, Manske PR. Involvement of ERK in BMP-2 induced osteoblastic differentiation of mesenchymal progenitor cell line C3H10T1/2. Biochem Biophys Res Commun. 2000;268:757–762.
Crossref Google Scholar
56

Warren SM, Brunet LJ, Harland RM, Economides AN, Longaker MT. The BMP antagonist noggin regulates cranial suture fusion. Nature. 2003;422:625–629.
Crossref Google Scholar
57

Cooper GM, Curry C, Barbano TE, et al. Noggin inhibits postoperative resynostosis in craniosynostotic rabbits. J Bone Miner Res. 2007;22:1046–1054.
Crossref Google Scholar
58

Nacamuli RP, Fong KD, Lenton KA, et al. Expression and possible mechanisms of regulation of BMP3 in rat cranial sutures. Plast Reconstr Surg. 2005;116:1353–1362.
Crossref Google Scholar
59

Lee MS, Lowe GN, Strong DD, Wergedal JE, Glackin CA. TWIST, a basic helix-loop-helix transcription factor, can regulate the human osteogenic lineage. J Cell Biochem. 1999;75:566–577.
Crossref Google Scholar
60

Gripp KW, Zackai EH, Stolle CA. Mutations in the human TWIST gene. Hum Mutat. 2000;15:150–155.
Crossref Google Scholar
61

Ting MC, Wu NL, Roybal PG, et al. EphA4 as an effector of Twist1 in the guidance of osteogenic precursor cells during calvarial bone growth and in craniosynostosis. Development. 2009;136:855–864.
Crossref Google Scholar
62

Twigg SR, Kan R, Babbs C, et al. Mutations of ephrin-B1 (EFNB1), a marker of tissue boundary formation, cause craniofrontonasal syndrome. Proc Natl Acad Sci USA. 2004;101:8652–8657.
Crossref Google Scholar
63

Fardellone P, Séjourné A, Paccou J, Goëb V. Bone remodelling markers in rheumatoid arthritis. Mediat Inflamm. 2014;2014:484280.
Crossref Google Scholar
64

Peng X, Guo W, Ren T, et al. Differential expression of the RANKL/RANK/OPG system is associated with bone metastasis in human non-small cell lung cancer. PLoS One. 2013;8:e58361.
Crossref Google Scholar
65

Asagiri M, Takayanagi H. The molecular understanding of osteoclast differentiation. Bone. 2007;40:251–264.
Crossref Google Scholar
66

Takayanagi H. Mechanistic insight into osteoclast differentiation in osteoimmunology. J Mol Med Berl. 2005;83:170–179.
Crossref Google Scholar
67

Leibbrandt A, Penninger JM. Novel functions of RANK(L) signaling in the immune system. Adv Exp Med Biol. 2010;658:77–94.
Crossref Google Scholar
68

Woo KM, Kim HM, Ko JS. Macrophage colony-stimulating factor promotes the survival of osteoclast precursors by up-regulating Bcl-X(L). Exp Mol Med. 2002;34:340–346.
Crossref Google Scholar
69

Tsuda E, Goto M, Mochizuki S, et al. Isolation of a novel cytokine from human fibroblasts that specifically inhibits osteoclastogenesis. Biochem Biophys Res Commun. 1997;234:137–142.
Crossref Google Scholar
70

Yun TJ, Tallquist MD, Aicher A, et al. Osteoprotegerin, a crucial regulator of bone metabolism, also regulates B cell development and function. J Immunol. 2001;166:1482–1491.
Crossref Google Scholar
71

Simonet WS, Lacey DL, Dunstan CR, et al. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell. 1997;89:309–319.
Crossref Google Scholar
72

Bucay N, Sarosi I, Dunstan CR, et al. osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev. 1998;12:1260–1268.
Crossref Google Scholar
73

Suzuki J, Ikeda T, Kuroyama H, et al. Regulation of osteoclastogenesis by three human RANKL isoforms expressed in NIH3T3 cells. Biochem Biophysical Res Commun. 2004;314:1021–1027.
Crossref Google Scholar
74

Anderson DM, Maraskovsky E, Billingsley WL, et al. A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature. 1997;390:175–179.
Crossref Google Scholar
75

Kong YY, Yoshida H, Sarosi I, et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999;397:315–323.
Crossref Google Scholar
76

Li J, Sarosi I, Yan XQ, et al. RANK is the intrinsic hematopoietic cell surface receptor that controls osteoclastogenesis and regulation of bone mass and calcium metabolism. Proc Natl Acad Sci USA. 2000;97:1566–1571.
Crossref Google Scholar
77

Kobayashi N, Kadono Y, Naito A, et al. Segregation of TRAF6-mediated signaling pathways clarifies its role in osteoclastogenesis. EMBO J. 2001;20:1271–1280.
Crossref Google Scholar
78

Gohda J, Akiyama T, Koga T, Takayanagi H, Tanaka S, Inoue J. RANK-mediated amplification of TRAF6 signaling leads to NFATc1 induction during osteoclastogenesis. EMBO J. 2005;24:790–799.
Crossref Google Scholar
79

Asagiri M, Sato K, Usami T, et al. Autoamplification of NFATc1 expression determines its essential role in bone homeostasis. J Exp Med. 2005;202:1261–1269.
Crossref Google Scholar
80

Kim Y, Sato K, Asagiri M, Morita I, Soma K, Takayanagi H. Contribution of nuclear factor of activated T cells c1 to the transcriptional control of immunoreceptor osteoclast-associated receptor but not triggering receptor expressed by myeloid cells-2 during osteoclastogenesis. J Biol Chem. 2005;280:32905–32913.
Crossref Google Scholar
81

Fuller K, Wong B, Fox S, Choi Y, Chambers TJ. TRANCE is necessary and sufficient for osteoblast-mediated activation of bone resorption in osteoclasts. J Exp Med. 1998;188:997–1001.
Crossref Google Scholar
82

Lacey DL, Timms E, Tan HL, et al. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998;93:165–176.
Crossref Google Scholar
83

Yasuda H, Shima N, Nakagawa N, et al. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci USA. 1998;95:3597–3602.
Crossref Google Scholar
84

Nakagawa N, Kinosaki M, Yamaguchi K, et al. RANK is the essential signaling receptor for osteoclast differentiation factor in osteoclastogenesis. Biochem Biophys Res Commun. 1998;253:395–400.
Crossref Google Scholar
85

Flick LM, Weaver JM, Ulrich-Vinther M, et al. Effects of receptor activator of NFkappaB (RANK) signaling blockade on fracture healing. J Orthop Res. 2003;21:676–684.
Crossref Google Scholar
86

Whyte MP, Mumm S. Heritable disorders of the RANKL/OPG/RANK signaling pathway. J Musculoskelet Neuronal Interact. 2004;4:254–267.
Google Scholar
87

Nakashima T, Wada T, Penninger JM. RANKL and RANK as novel therapeutic targets for arthritis. Curr Opin Rheumatol. 2003;15:280–287.
Crossref Google Scholar
88

Sobacchi C, Schulz A, Coxon FP, Villa A, Helfrich MH. Osteopetrosis: genetics, treatment and new insights into osteoclast function. Nat Rev Endocrinol. 2013;9:522–536.
Crossref Google Scholar
89
Krimmel M, Niemann G, Will B, Reinert S. Surgical correction of craniosynostosis in malignant osteopetrosis. J Craniofac Surg. 2004;15:218–220. discussion 221.
Crossref
90

Elster AD, Theros EG, Key LL, Chen MY. Cranial imaging in autosomal recessive osteopetrosis. Part Ⅰ. Facial bones and calvarium. Radiology. 1992;183:129–135.
Crossref Google Scholar
91

Elster AD, Theros EG, Key LL, Chen MY. Cranial imaging in autosomal recessive osteopetrosis. Part Ⅱ. Skull base and brain. Radiology. 1992;183:137–144.
Crossref Google Scholar
92

Lo Iacono N, Blair HC, Poliani PL, et al. Osteopetrosis rescue upon RANKL administration to Rankl(-/-) mice: a new therapy for human RANKL-dependent ARO. J Bone Miner Res. 2012;27:2501–2510.
Crossref Google Scholar
93

Lee JC, Spiguel L, Shenaq DS, et al. Role of RANK-RANKL-OPG axis in cranial suture homeostasis. J Craniofacial Surg. 2011;22:699–705.
Crossref Google Scholar
94

Szpalski C, Wetterau M, Barr J, Warren SM. Bone tissue engineering: current strategies and techniques–part Ⅰ: Scaffolds. Tissue Eng Part B Rev. 2012;18:246–257.
Crossref Google Scholar
95

Szpalski C, Sagebin F, Barbaro M, Warren SM. The influence of environmental factors on bone tissue engineering. J Biomed Mater Res B Appl Biomater. 2013;101:663–675.
Crossref Google Scholar
96

Vacanti CA, Bonassar LJ, Vacanti MP, Shufflebarger J. Replacement of an avulsed phalanx with tissue-engineered bone. N Engl J Med. 2001;344:1511–1514.
Crossref Google Scholar
97

Warnke PH, Springer IN, Wiltfang J, et al. Growth and transplantation of a custom vascularised bone graft in a man. Lancet. 2004;364:766–770.
Crossref Google Scholar
98

Warnke PH, Wiltfang J, Springer I, et al. Man as living bioreactor: fate of an exogenously prepared customized tissue-engineered mandible. Biomaterials. 2006;27:3163–3167.
Crossref Google Scholar
99

Morishita T, Honoki K, Ohgushi H, Kotobuki N, Matsushima A, Takakura Y. Tissue engineering approach to the treatment of bone tumors: three cases of cultured bone grafts derived from patients' mesenchymal stem cells. Artif Organs. 2006;30:115–118.
Crossref Google Scholar
100

Quarto R, Mastrogiacomo M, Cancedda R, et al. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med. 2001;344:385–386.
Crossref Google Scholar
101

Schimming R, Schmelzeisen R. Tissue-engineered bone for maxillary sinus augmentation. J Oral Maxillofac Surg. 2004;62:724–729.
Crossref Google Scholar
102

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.
Crossref Google Scholar
103

Hibi H, Yamada Y, Ueda M, Endo Y. Alveolar cleft osteoplasty using tissue-engineered osteogenic material. Int J Oral Maxillofac Surg. 2006;35:551–555.
Crossref Google Scholar
104

Dickinson BP, Ashley RK, Wasson KL, et al. Reduced morbidity and improved healing with bone morphogenic protein-2 in older patients with alveolar cleft defects. Plast Reconstr Surg. 2008;121:209–217.
Crossref Google Scholar
105

Fallucco MA, Carstens MH. Primary reconstruction of alveolar clefts using recombinant human bone morphogenic protein-2: clinical and radiographic outcomes. J Craniofac Surg. 2009;20(suppl 2):1759–1764.
Crossref Google Scholar
106

Yee KS, Nguyen PD, Andrews BT, Lee JC, Bradley JP. Abstract 4: decreased secondary bone grafting but poorer midface growth after primary alveolar cleft repair with gingivoperiosteoplasty and rhBMP-2. Plast Reconstr Surg. 2014;133(suppl 4):975.
Crossref Google Scholar
107

Zheng YH, Su K, Jian YT, Kuang SJ, Zhang ZG. Basic fibroblast growth factor enhances osteogenic and chondrogenic differentiation of human bone marrow mesenchymal stem cells in coral scaffold constructs. J Tissue Eng Regen Med. 2011;5:540–550.
Crossref Google Scholar
108

Maegawa N, Kawamura K, Hirose M, Yajima H, Takakura Y, Ohgushi H. Enhancement of osteoblastic differentiation of mesenchymal stromal cells cultured by selective combination of bone morphogenetic protein-2 (BMP-2) and fibroblast growth factor-2 (FGF-2). J Tissue Eng Regen Med. 2007;1:306–313.
Crossref Google Scholar
109

Kwan MD, Sellmyer MA, Quarto N, Ho AM, Wandless TJ, Longaker MT. Chemical control of FGF-2 release for promoting calvarial healing with adipose stem cells. J Biol Chem. 2011;286:11307–11313.
Crossref Google Scholar
110
Quarto N, Senarath-Yapa K, Renda A, Longaker MT. TWIST1 silencing enhances in vitro and in vivo osteogenic differentiation of human adipose derived stem cells (hASCs) by triggering activation of BMP-ERK/FGF signaling and TAZ upregulation. Stem Cells. 2014. [Epub ahead of print]. http://dx.doi.org/10.1002/stem.1907.
Crossref
111

Jiang WW, Su SH, Eberhart RC, Tang L. Phagocyte responses to degradable polymers. J Biomed Mater Res A. 2007;82:492–497.
Crossref Google Scholar
112

Bergsma EJ, Rozema FR, Bos RR, de Bruijn WC. Foreign body reactions to resorbable poly(L-lactide) bone plates and screws used for the fixation of unstable zygomatic fractures. J Oral Maxillofac Surg. 1993;51:666–670.
Crossref Google Scholar
Genes & Diseases
Volume 2 Issue 1,
January 2015
Pages 57-68
DOI: 10.1016/j.gendis.2014.12.004
Cite this article:
Maxhimer JB, Bradley JP, Lee JC. Signaling pathways in osteogenesis and osteoclastogenesis: Lessons from cranial sutures and applications to regenerative medicine. Genes & Diseases, 2015, 2(1): 57-68. https://doi.org/10.1016/j.gendis.2014.12.004

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Received: 09 December 2014
Accepted: 31 December 2014
Published: 09 January 2015
© 2015, Chongqing Medical University.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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