Nell-1-induced bone regeneration in calvarial defects

American Journal of Pathology

Volumn 169, Issue 3, 2006, Pages 903-915

  Aghaloo, Tara ^a   Cowan, Catherine M ^b   Chou, Yu Fen ^b   Zhang, Xinli ^a   Lee, Haofu ^a   Miao, Steve ^a   Hong, Nichole ^a   Kuroda, Shun'ichi ^e   Wu, Benjamin ^a,b,c   Ting, Kang ^a   Soo, Chia ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California   (United States)

^c UCLA SCHOOL OF DENTISTRY   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; NERVE PROTEIN; OSTEOCALCIN; OSTEOGENIC PROTEIN 1; PROTEIN NELL1; SIALOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE GROWTH; BONE REGENERATION; CALVARIA; CELL DIFFERENTIATION; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; CRANIOFACIAL SYNOSTOSIS; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

EID: 33748807766     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.051210     Document Type: Article

References (73)

1. Canady JW, Zeitler DP, Thompson SA, Nicholas CD: Suitability of the iliac crest as a site for harvest of autogenous bone grafts. Cleft Palate Craniofac J 1993, 30:579-581
2. Schlegel KA, Donath K, Rupprecht S, Falk S, Zimmermann R, Felszeghy E, Wiltfang J: De novo bone formation using bovine collagen and platelet-rich plasma. Biomaterials 2004, 25:5387-5393
3. Kang Q, Sun MH, Cheng H, Peng Y, Montag AG, Deyrup AT, Jiang W, Luu HH, Luo J, Szatkowski JP, Vanichakarn P, Park JY, Li Y, Haydon RC, He TC: Characterization of the distinct orthotopic bone-forming activity of 14 BMPs using recombinant adenovirus-mediated gene delivery. Gene Ther 2004, 11:1312-1320
4. Boden SD, Kang J, Sandhu H, Heller JG: Use of recombinant human bone morphogenetic protein-2 to achieve posterolateral lumbar spine fusion in humans: a prospective, randomized clinical pilot trial: 2002 Volvo Award in clinical studies. Spine 2002, 27:2662-2673
5. Valentin-Opran A, Wozney J, Csimma C, Lilly L, Riedel GE: Clinical evaluation of recombinant human bone morphogenetic protein-2. Clin Orthop 2002, 1:110-120
6. Franceschi RT, Xiao G: Regulation of the osteoblast-specific transcription factor, Runx2: responsiveness to multiple signal transduction pathways. J Cell Biochem 2003, 88:446-454
7. Zhang X, Kuroda S, Carpenter D, Nishimura I, Soo C, Moats R, Iida K, Wisner E, Hu FY, Miao S, Beanes S, Dang C, Vastardis H, Longaker M, Tanizawa K, Kanayama N, Saito N, Ting K: Craniosynostosis in transgenic mice overexpressing Nell-1. J Clin Invest 2002, 110:861-870
8. Ting K, Vastardis H, Mulliken JB, Soo C, Tieu A, Do H, Kwong E, Bertolami CN, Kawamoto H, Kuroda S, Longaker MT: Human NELL-1 expressed in unilateral coronal synostosis. J Bone Miner Res 1999, 14:80-89
9. Watanabe TK, Katagiri T, Suzuki M, Shimizu F, Fujiwara T, Kanemoto N, Nakamura Y, Hirai Y, Maekawa H, Takahashi E: Cloning and characterization of two novel human cDNAs (NELL1 and NELL2) encoding proteins with six EGF-like repeats. Genomics 1996, 38:273-276
10. Kuroda S, Oyasu M, Kawakami M, Kanayama N, Tanizawa K, Saito N, Abe T, Matsuhashi S, Ting K: Biochemical characterization and expression analysis of neural thrombospondin-1-like proteins NELL1 and NELL2. Biochem Biophys Res Commun 1999, 265:79-86
11. Desai J, Hughes L, Millsaps J, Stanford B, Kerley M, Carpenter D, Rinchik E, Culiat C: NELL-1, a gene coding for a novel PKC-binding protein is a candidate for late-gestation recessive lethal mutations at the L7R6 locus. Presented at The 16th International Mouse Genome Conference, San Antonio, TX, 2002
12. Kuroda S, Tanizawa K: Involvement of epidermal growth factor-like domain of NELL proteins in the novel protein-protein interaction with protein kinase C. Biochem Biophys Res Commun 1999, 265:752-757
13. Zhang X, Carpenter D, Bokui N, Soo C, Miao S, Truong T, Wu B, Chen I, Vastardis H, Tanizawa K, Kuroda S, Ting K: Overexpression of Nell-1, a craniosynostosis-associated gene, induces apoptosis in osteoblasts during craniofacial development. J Bone Miner Res 2003, 18:2126-2134
14. Truong S, Zhang X, Miao Y, Chiu R, Ting K: Cbfa1 regulation of the human Nell-1 promoter. J Dent Res 2004, 83:1307
15. Truong S, Zhang X, Pathmanathan D, Soo C, Ting K: Runt homology domain transcription factor Runx2 mediates induction of the Nell-1 promoter. J Biol Chem (in press)
16. Liu YH, Kundu R, Wu L, Luo W, Ignelzi Jr MA, Snead ML, Maxson Jr RE: Premature suture closure and ectopic cranial bone in mice expressing Msx2 transgenes in the developing skull. Proc Natl Acad Sci USA 1995, 92:6137-6141
17. Zhou YX, Xu X, Chen L, Li C, Brodie SG, Deng CX: A Pro250Arg substitution in mouse Fgfr1 causes increased expression of Cbfa1 and premature fusion of calvarial sutures. Hum Mol Genet 2000, 9:2001-2008
18. Bonewald L: Transforming growth factor-beta. Principles of Bone Biology. Edited by Bilezikian J, Riaisz L, Rodan G, San Diego, Academic Press, 2002, pp 903
19. Vehof JW, Fisher JP, Dean D, van der Waerden JP, Spauwen PH, Mikos AG, Jansen JA: Bone formation in transforming growth factor beta-1-coated porous poly(propylene fumarate) scaffolds. J Biomed Mater Res 2002, 60:241-251
20. Gosain AK, Song L, Yu P, Mehrara BJ, Maeda CY, Gold LI, Longaker MT: Osteogenesis in cranial defects: reassessment of the concept of critical size and the expression of TGF-beta isoforms. Plast Reconstr Surg 2000, 106:360-372
21. Gong Z, Zhou S, Cao J, Gu X: Effects of recombinant human basic fibroblast growth factor on cell proliferation during mandibular fracture healing in rabbits. Chin J Traumatol 2001, 4:110-112
22. Rosado E, Schwartz Z, Sylvia VL, Dean DD, Boyan BD: Transforming growth factor-beta1 regulation of growth zone chondrocytes is mediated by multiple interacting pathways. Biochim Biophys Acta 2002, 1590:1-15
23. Greenwald JA, Mehrara BJ, Spector JA, Warren SM, Grisera FE, Fagenholz PJ, Bouletreau PJ, Longaker MT: Regional differentiation of cranial suture-associated dura mater in vivo and in vitro: implications for suture fusion and patency. J Bone Miner Res 2000, 15:2413-2430
24. Heid CA, Stevens J, Livak KJ, Williams PM: Real time quantitative PCR. Genome Res 1996, 6:986-994
25. Cowan C, Shi Y, Aalami O, Chou Y, Mari C, Thomas R, Quarto N, Contag C, Wu B, Longaker M: Adipose-derived adult stromal cells heal critical-sized mouse calvarial defects. Nature Biotechnol 2004, 22:560-567
26. Berger F, Lee YP, Loening AM, Chatziioannou A, Freedland SJ, Leahy R, Lieberman JR, Belldegrun AS, Sawyers CL, Gambhir SS: Whole-body skeletal imaging in mice utilizing microPET: optimization of reproducibility and applications in animal models of bone disease. Eur J Nucl Med Mol Imaging 2002, 29:1225-1236
27. Borah B, Dufresne TE, Cockman MD, Gross GJ, Sod EW, Myers WR, Combs KS, Higgins RE, Pierce SA, Stevens ML: Evaluation of changes in trabecular bone architecture and mechanical properties of minipig vertebrae by three-dimensional magnetic resonance microimaging and finite element modeling. J Bone Miner Res 2000, 15:1786-1797
28. Vehof JW, Mahmood J, Takita H, van't Hof MA, Kuboki Y, Spauwen PH, Jansen JA: Ectopic bone formation in titanium mesh loaded with bone morphogenetic protein and coated with calcium phosphate. Plast Reconstr Surg 2001, 108:434-443
29. Bouletreau PJ, Steinbrech D, Spector JA, Warren SM, Greenwald JA, Mehrara BJ, Detch RC, Longaker MT: Gene expression of transforming growth factor-beta 3 and tissue inhibitor of metalloproteinase type 1 during membranous bone healing in rats. J Craniofac Surg 2000, 11:521-526
30. Lee KS, Hong SH, Bae SC: Both the Smad and p38 MAPK pathways play a crucial role in Runx2 expression following induction by transforming growth factor-beta and bone morphogenetic protein. Oncogene 2002, 21:7156-7163
31. Cowan CM, Soo C, Ting K, Wu B: Evolving concepts in bone tissue engineering. Curr Top Dev Biol 2005, 66:239-285
32. Peng Y, Kang Q, Cheng H, Li X, Sun MH, Jiang W, Luu HH, Park JY, Haydon RC, He TC: Transcriptional characterization of bone morphogenetic proteins (BMPs)-mediated osteogenic signaling. J Cell Biochem 2003, 90:1149-1165
33. Koch H, Jadlowiec JA, Campbell PG: Insulin-like growth factor-I induces early osteoblast gene expression in human mesenchymal stem cells. Stem Cells Dev 2005, 14:621-631
34. Skillington J, Choy L, Derynck R: Bone morphogenetic protein and retinoic acid signaling cooperate to induce osteoblast differentiation of preadipocytes. J Cell Biol 2002, 159:135-146
35. Owen TA, Aronow M, Shalhoub V, Barone LM, Wilming L, Tassinari MS, Kennedy MB, Pockwinse S, Lian JB, Stein GS: Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol 1990, 143:420-430
36. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B: The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 2002, 108:17-29
37. Frazza EJ, Schmitt EE: A new absorbable suture. J Biomed Mater Res 1971, 5:43-58
38. Bessho K, Carnes DL, Cavin R, Ong JL: Experimental studies on bone induction using low-molecular-weight poly (DL-lactide-co-glycolide) as a carrier for recombinant human bone morphogenetic protein-2. J Biomed Mater Res 2002, 61:61-65
39. Boyan BD, Lohmann CH, Somers A, Niederauer GG, Wozney JM, Dean DD, Carnes Jr DL, Schwartz Z: Potential of porous poly-D,L-lactide-co-glycolide particles as a carrier for recombinant human bone morphogenetic protein-2 during osteoinduction in vivo. J Biomed Mater Res 1999, 46:51-59
40. Hollinger JO, Leong K: Poly(alpha-hydroxy acids): carriers for bone morphogenetic proteins. Biomaterials 1996, 17:187-194
41. Cowan CM, Aalami OO, Shi YY, Chou YF, Marl C, Thomas R, Quarto N, Nacamuli RP, Contag CH, Wu B, Longaker MT: Bone morphogenetic protein 2 and retinoic acid accelerate in vivo bone formation, osteoclast recruitment, and bone turnover. Tissue Eng 2005, 11:645-658
42. Hyun SJ, Han DK, Choi SH, Chai JK, Cho KS, Kim CK, Kim CS: Effect of recombinant human bone morphogenetic protein-2, -4, and -7 on bone formation in rat calvarial defects. J Periodontol 2005, 76:1667-1674
43. Chen J, Shapiro HS, Sodek J: Development expression of bone sialoprotein mRNA in rat mineralized connective tissues. J Bone Miner Res 1992, 7:987-997
44. Warren SM, Brunet LJ, Harland RM, Economides AN, Longaker MT: The BMP antagonist noggin regulates cranial suture fusion. Nature 2003, 422:625-629
45. Abreu JG, Ketpura NI, Reversade B, De Robertis EM: Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat Cell Biol 2002, 4:599-604
46. Clezardin P, Lawler J, Amiral J, Quentin G, Delmas P: Identification of cell adhesive active sites in the N-terminal domain of thrombospondin-1. Biochem J 1997, 321:819-827
47. Fromigue O, Modrowski D, Marie PJ: Growth factors and bone formation in osteoporosis: roles for fibroblast growth factor and transforming growth factor beta. Curr Pharm Des 2004, 10:2593-2603
48. Ahrens M, Ankenbauer T, Schroder D, Hollnagel A, Mayer H, Gross G: Expression of human bone morphogenetic proteins-2 or -4 in murine mesenchymal progenitor C3H10T1/2 cells induces differentiation into distinct mesenchymal cell lineages. DNA Cell Biol 1993, 12:871-880
49. Katagiri T, Yamaguchi A, Komaki M, Abe E, Takahashi N, Ikeda T, Rosen V, Wozney JM, Fujisawa-Sehara A, Suda T: Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol 1994, 127:1755-1766
50. Lian JB, Javed A, Zaidi SK, Lengner C, Montecino M, van Wijnen AJ, Stein JL, Stein GS: Regulatory controls for osteoblast growth and differentiation: role of Runx/Cbfa/AML factors. Crit Rev Eukaryot Gene Expr 2004, 14:1-41
51. Yoshida CA, Furuichi T, Fujita T, Fukuyama R, Kanatani N, Kobayashi S, Satake M, Takada K, Komori T: Core-binding factor beta interacts with Runx2 and is required for skeletal development. Nat Genet 2002, 32:633-638
52. Lenton KA, Nacamuli RP, Wan DC, Helms JA, Longaker MT: Cranial suture biology. Curr Top Dev Biol 2005, 66:287-328
53. Vukicevic S, Luyten FP, Reddi AH: Osteogenin inhibits proliferation and stimulates differentiation in mouse osteoblast-like cells (MC3T3-E1). Biochem Biophys Res Commun 1990, 166:750-756
54. McCauley LK, Koh AJ, Beecher CA, Cui Y, Decker JD, Franceschi RT: Effects of differentiation and transforming growth factor beta 1 on PTH/PTHrP receptor mRNA levels in MC3T3-E1 cells. J Bone Miner Res 1995, 10:1243-1255
55. Blanquaert F, Barritault D, Caruelle JP: Effects of heparan-like polymers associated with growth factors on osteoblast proliferation and phenotype expression. J Biomed Mater Res 1999, 44:63-72
56. Xiao G, Jiang D, Gopalakrishnan R, Franceschi RT: Fibroblast growth factor 2 induction of the osteocalcin gene requires MARK activity and phosphorylation of the osteoblast transcription factor, Cbfa1/Runx2. J Biol Chem 2002, 277:36181-36187
57. Vaes BL, Dechering KJ, Feijen A, Hendriks JM, Lefevre C, Mummery CL, Olijve W, van Zoelen EJ, Steegenga WT: Comprehensive microarray analysis of bone morphogenetic protein 2-induced osteoblast differentiation resulting in the identification of novel markers for bone development. J Bone Miner Res 2002, 17:2106-2118
58. Kozawa O, Suzuki A, Uematsu T: Basic fibroblast growth factor induces interleukin-6 synthesis in osteoblasts: autoregulation by protein kinase C. Cell Signal 1997, 9:463-468
59. Hay E, Lemonnier J, Fromigue O, Marie PJ: Bone morphogenetic protein-2 promotes osteoblast apoptosis through a Smad-independent, protein kinase C-dependent signaling pathway. J Biol Chem 2001, 276:29028-29036
60. Celil AB, Campbell PG: BMP-2 and IGF-I mediate Osx expression in human mesenchymal stem cells via the MAPK and PKD signaling pathways. J Biol Chem 2005, 280:31353-31359
61. Lee MH, Kwon TG, Park HS, Wozney JM, Ryoo HM: BMP-2-induced Osterix expression is mediated by Dlx5 but is independent of Runx2. Biochem Biophys Res Commun 2003, 309:689-694
62. Celil AB, Hollinger JO, Campbell PG: Osx transcriptional regulation is mediated by additional pathways to BMP2/Smad signaling. J Cell Biochem 2005, 95:518-528
63. Lee JY, Musgrave D, Pelinkovic D, Fukushima K, Cummins J, Usas A, Robbins P, Fu FH, Huard J: Effect of bone morphogenetic protein-2-expressing muscle-derived cells on healing of critical-sized bone defects in mice. J Bone Joint Surg Am 2001, 83A:1032-1039
64. Mehrara BJ, Spector JA, Greenwald JA, Ueno H, Longaker MT: Adenovirus-mediated transmission of a dominant negative transforming growth factor-beta receptor inhibits in vitro mouse cranial suture fusion. Plast Reconstr Surg 2002, 110:506-514
65. Andriano KP, Chandrashekar B, McEnery K, Dunn RL, Moyer K, Balliu CM, Holland KM, Garrett S, Huffer WE: Preliminary in vivo studies on the osteogenic potential of bone morphogenetic proteins delivered from an absorbable puttylike polymer matrix. J Biomed Mater Res 2000, 53:36-43
66. Gysin R, Wergedal JE, Sheng MH, Kasukawa Y, Miyakoshi N, Chen ST, Peng H, Lau KH, Mohan S, Baylink DJ: Ex vivo gene therapy with stromal cells transduced with a retroviral vector containing the BMP4 gene completely heals critical size calvarial defect in rats. Gene Ther 2002, 9:991-999
67. Cheng H, Jiang W, Phillips FM, Haydon RC, Peng Y, Zhou L, Luu HH, An N, Breyer B, Vanichakarn P, Szatkowski JP, Park JY, He TC: Osteogenic activity of the fourteen types of human bone morphogenetic proteins (BMPs). J Bone Joint Surg Am 2003, 85A:1544-1552
68. Fujisawa R, Kuboki Y: Affinity of bone sialoprotein and several other bone and dentin acidic proteins to collagen fibrils. Calcif Tissue Int 1992, 51:438-442
69. Oldberg A, Franzen A, Heinegard D: The primary structure of a cell-binding bone sialoprotein. J Biol Chem 1988, 263:19430-19432
70. Wang J, Glimcher MJ, Mah J, Zhou HY, Salih E: Expression of bone microsomal casein kinase II, bone sialoprotein, and osteopontin during the repair of calvarial defects. Bone 1998, 22:621-628
71. Hoang QQ, Sicheri F, Howard AJ, Yang DS: Bone recognition mechanism of porcine osteocalcin from crystal structure. Nature 2003, 425:977-980
72. Cowan C, Cheng S, Ting K, Soo C, Walder B, Wu B, Kuroda S, Zhang X: Nell-1 induced bone formation within the distracted intermaxillary suture. Bone 2005, 38:48-58
73. Moreira-Gonzalez A, Jackson IT, Miyawaki T, Barakat K, DiNick V: Clinical outcome in cranioplasty: critical review in long-term follow-up. J Craniofac Surg 2003, 14:144-153