SHP2 Regulates Chondrocyte Terminal Differentiation, Growth Plate Architecture and Skeletal Cell Fates

PLoS Genetics

Volumn 10, Issue 5, 2014, Pages

  Bowen, Margot E ^a   Ayturk, Ugur M ^a   Kurek, Kyle C ^a   Yang, Wentian ^b   Warman, Matthew L ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN TYROSINE PHOSPHATASE SHP 2; PTPN11 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE CELL; CARTILAGE CELL; CARTILAGE TUMOR; CELL CULTURE; CELL DIFFERENTIATION; CELL FATE; CELL MATURATION; CONTROLLED STUDY; ENCHONDROMA; ENZYME INHIBITION; EXOSTOSIS; FIBROBLAST; GENE INACTIVATION; GROWTH PLATE; HUMAN; HUMAN TISSUE; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; METACHONDROMATOSIS; MOUSE; NEWBORN; NONHUMAN; OSSIFICATION; PROTEIN DEPLETION; PTPN11 GENE; VERTEBRA; ANIMAL; BONE DEVELOPMENT; BONE TUMOR; CARTILAGE; CHONDROGENESIS; CHONDROMA; CHONDROMATOSIS; GENETICS; HEREDITARY MULTIPLE EXOSTOSIS; METABOLISM; PARACRINE SIGNALING; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BONE NEOPLASMS; CARTILAGE; CELL DIFFERENTIATION; CHONDROCYTES; CHONDROGENESIS; CHONDROMA; CHONDROMATOSIS; EXOSTOSES; EXOSTOSES, MULTIPLE HEREDITARY; GROWTH PLATE; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; OSTEOGENESIS; PARACRINE COMMUNICATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11;

EID: 84901596293     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004364     Document Type: Article

References (55)

1. Romeo S, Hogendoorn PCW, Dei Tos AP, (2009) Benign cartilaginous tumors of bone: from morphology to somatic and germ-line genetics. Adv Anat Pathol 16: 307-315 doi:10.1097/PAP.0b013e3181b506a1.
2. Bowen ME, Boyden ED, Holm IA, Campos-Xavier B, Bonafé L, et al. (2011) Loss-of-function mutations in PTPN11 cause metachondromatosis, but not Ollier disease or Maffucci syndrome. PLoS Genet 7: e1002050 doi:10.1371/journal.pgen.1002050.
3. Sobreira NLM, Cirulli ET, Avramopoulos D, Wohler E, Oswald GL, et al. (2010) Whole-genome sequencing of a single proband together with linkage analysis identifies a Mendelian disease gene. PLoS Genet 6: e1000991 doi:10.1371/journal.pgen.1000991.
4. Grossmann KS, Rosário M, Birchmeier C, Birchmeier W, (2010) The tyrosine phosphatase Shp2 in development and cancer. Adv Cancer Res 106: 53-89 doi:10.1016/S0065-230X(10)06002-1.
5. Amary MF, Bacsi K, Maggiani F, Damato S, Halai D, et al. (2011) IDH1 and IDH2 mutations are frequent events in central chondrosarcoma and central and periosteal chondromas but not in other mesenchymal tumours. The Journal of Pathology 224: 334-343 doi:10.1002/path.2913.
6. Amary MF, Damato S, Halai D, Eskandarpour M, Berisha F, et al. (2011) Ollier disease and Maffucci syndrome are caused by somatic mosaic mutations of IDH1 and IDH2. Nature Genetics 43: 1262-1265 doi:10.1038/ng.994.
7. Pansuriya TC, van Eijk R, d' Adamo P, van Ruler MAJH, Kuijjer ML, et al. (2011) Somatic mosaic IDH1 and IDH2 mutations are associated with enchondroma and spindle cell hemangioma in Ollier disease and Maffucci syndrome. Nature Genetics 43: 1256-1261 doi:10.1038/ng.1004.
8. Jennes I, Pedrini E, Zuntini M, Mordenti M, Balkassmi S, et al. (2009) Multiple osteochondromas: mutation update and description of the multiple osteochondromas mutation database (MOdb). Hum Mutat 30: 1620-1627 doi:10.1002/humu.21123.
9. Yang W, Klaman LD, Chen B, Araki T, Harada H, et al. (2006) An Shp2/SFK/Ras/Erk Signaling Pathway Controls Trophoblast Stem Cell Survival. Developmental Cell 10: 317-327 doi:10.1016/j.devcel.2006.01.002.
10. Bauler TJ, Kamiya N, Lapinski PE, Langewisch E, Mishina Y, et al. (2011) Development of severe skeletal defects in induced SHP-2-deficient adult mice: a model of skeletal malformation in humans with SHP-2 mutations. Dis Model Mech 4: 228-239 doi:10.1242/dmm.006130.
11. Yang W, Wang J, Moore DC, Liang H, Dooner M, et al. (2013) Ptpn11 deletion in a novel progenitor causes metachondromatosis by inducing hedgehog signalling. Nature 499: 491-495 doi:10.1038/nature12396.
12. Kim HK, Feng G-S, Chen D, King PD, Kamiya N, (2014) Targeted disruption of shp2 in chondrocytes leads to metachondromatosis with multiple cartilaginous protrusions. J Bone Miner Res 29: 761-769 doi:10.1002/jbmr.2062.
13. Kim HKW, Aruwajoye O, Sucato D, Richards BS, Feng G-S, et al. (2013) Induction of SHP2 deficiency in chondrocytes causes severe scoliosis and kyphosis in mice. Spine 38: E1307-1312 doi:10.1097/BRS.0b013e3182a3d370.
14. Matsushita T, Chan YY, Kawanami A, Balmes G, Landreth GE, et al. (2009) Extracellular Signal-Regulated Kinase 1 (ERK1) and ERK2 Play Essential Roles in Osteoblast Differentiation and in Supporting Osteoclastogenesis. Molecular and Cellular Biology 29: 5843-5857 doi:10.1128/MCB.01549-08.
15. Sebastian A, Matsushita T, Kawanami A, Mackem S, Landreth GE, et al. (2011) Genetic inactivation of ERK1 and ERK2 in chondrocytes promotes bone growth and enlarges the spinal canal. Journal of Orthopaedic Research 29: 375-379 doi:10.1002/jor.21262.
16. Kato Y, Iwamoto M, Koike T, Suzuki F, Takano Y, (1988) Terminal differentiation and calcification in rabbit chondrocyte cultures grown in centrifuge tubes: regulation by transforming growth factor beta and serum factors. Proc Natl Acad Sci USA 85: 9552-9556.
17. Chen K-S, Tatarczuch L, Ahmed Y, Huang HH, Mirams M, et al. (2010) Identification of light and dark hypertrophic chondrocytes in mouse and rat chondrocyte pellet cultures. Tissue and Cell 42: 121-128 doi:10.1016/j.tice.2010.02.003.
18. Nishimura R, Hata K, Ono K, Amano K, Takigawa Y, et al. (2012) Regulation of endochondral ossification by transcription factors. Front Biosci 17: 2657-2666.
19. Oshlack A, Robinson MD, Young MD, (2010) From RNA-seq reads to differential expression results. Genome Biol 11: 220 doi:10.1186/gb-2010-11-12-220.
20. Zhang H, (2003) Profiling genes expressed in human fetal cartilage using 13,155 expressed sequence tags. Osteoarthritis and Cartilage 11: 309-319 doi:10.1016/S1063-4584(03)00032-3.
21. Miedlich SU, Zalutskaya A, Zhu ED, Demay MB, (2010) Phosphate-induced Apoptosis of Hypertrophic Chondrocytes Is Associated with a Decrease in Mitochondrial Membrane Potential and Is Dependent upon Erk1/2 Phosphorylation. Journal of Biological Chemistry 285: 18270-18275 doi:10.1074/jbc.M109.098616.
22. De Andrea CE, Wiweger MI, Bovée JVMG, Romeo S, Hogendoorn PCW, (2012) Peripheral chondrosarcoma progression is associated with increased type X collagen and vascularisation. Virchows Arch 460: 95-102 doi:10.1007/s00428-011-1168-9.
23. Huch K, Mordstein V, Stöve J, Nerlich AG, Amholdt H, et al. (2002) Expression of collagen type I, II, X and Ki-67 in osteochondroma compared to human growth plate cartilage. Eur J Histochem 46: 249-258.
24. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, et al. (2004) TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303: 848-851 doi:10.1126/science.1090922.
25. Tsutsumi R, Xie C, Wei X, Zhang M, Zhang X, et al. (2009) PGE2 signaling through the EP4 receptor on fibroblasts upregulates RANKL and stimulates osteolysis. J Bone Miner Res 24: 1753-1762 doi:10.1359/jbmr.090412.
26. Trimboli AJ, Cantemir-Stone CZ, Li F, Wallace JA, Merchant A, et al. (2009) Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 461: 1084-1091 doi:10.1038/nature08486.
27. Inoue T, Takenaka T, Hayashi M, Monkawa T, Yoshino J, et al. (2010) Fibroblast expression of an IκB dominant-negative transgene attenuates renal fibrosis. J Am Soc Nephrol 21: 2047-2052 doi:10.1681/ASN.2010010003.
28. Hopyan S, Gokgoz N, Poon R, Gensure RC, Yu C, et al. (2002) A mutant PTH/PTHrP type I receptor in enchondromatosis. Nature Genetics 30: 306-310 doi:10.1038/ng844.
29. Ho L, Ali SA, Al-Jazrawe M, Kandel R, Wunder JS, et al. (2013) Primary cilia attenuate hedgehog signalling in neoplastic chondrocytes. Oncogene 32: 5388-5396 doi:10.1038/onc.2012.588.
30. Douis H, Davies AM, James SL, Kindblom LG, Grimer RJ, et al. (2012) Can MR imaging challenge the commonly accepted theory of the pathogenesis of solitary enchondroma of long bone? Skeletal Radiology 41: 1537-1542 doi:10.1007/s00256-012-1387-4.
31. Lapinski PE, Meyer MF, Feng G-S, Kamiya N, King PD, (2013) Deletion of SHP-2 in mesenchymal stem cells causes growth retardation, limb and chest deformity, and calvarial defects in mice. Dis Model Mech 6: 1448-1458 doi:10.1242/dmm.012849.
32. Jones KB, Piombo V, Searby C, Kurriger G, Yang B, et al. (2010) A mouse model of osteochondromagenesis from clonal inactivation of Ext1 in chondrocytes. Proc Natl Acad Sci USA 107: 2054-2059 doi:10.1073/pnas.0910875107.
33. Lai LP, Mitchell J, (2005) Indian hedgehog: Its roles and regulation in endochondral bone development. Journal of Cellular Biochemistry 96: 1163-1173 doi:10.1002/jcb.20635.
34. Jacob AL, Smith C, Partanen J, Ornitz DM, (2006) Fibroblast growth factor receptor 1 signaling in the osteo-chondrogenic cell lineage regulates sequential steps of osteoblast maturation. Dev Biol 296: 315-328 doi:10.1016/j.ydbio.2006.05.031.
35. Wang K, Yamamoto H, Chin JR, Werb Z, Vu TH, (2004) Epidermal growth factor receptor-deficient mice have delayed primary endochondral ossification because of defective osteoclast recruitment. J Biol Chem 279: 53848-53856 doi:10.1074/jbc.M403114200.
36. Colvin JS, Bohne BA, Harding GW, McEwen DG, Ornitz DM, (1996) Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nat Genet 12: 390-397 doi:10.1038/ng0496-390.
37. Deng C, Wynshaw-Boris A, Zhou F, Kuo A, Leder P, (1996) Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell 84: 911-921.
38. Hattori T, Muller C, Gebhard S, Bauer E, Pausch F, et al. (2010) SOX9 is a major negative regulator of cartilage vascularization, bone marrow formation and endochondral ossification. Development 137: 901-911 doi:10.1242/dev.045203.
39. Salie R, Kneissel M, Vukevic M, Zamurovic N, Kramer I, et al. (2010) Ubiquitous overexpression of Hey1 transcription factor leads to osteopenia and chondrocyte hypertrophy in bone. Bone 46: 680-694 doi:10.1016/j.bone.2009.10.022.
40. Amano K, Ichida F, Sugita A, Hata K, Wada M, et al. (2008) Msx2 Stimulates Chondrocyte Maturation by Controlling Ihh Expression. Journal of Biological Chemistry 283: 29513-29521 doi:10.1074/jbc.M803681200.
41. Ferrari D, Kosher RA, (2002) Dlx5 Is a Positive Regulator of Chondrocyte Differentiation during Endochondral Ossification. Developmental Biology 252: 257-270 doi:10.1006/dbio.2002.0862.
42. Liu T, Gao Y, Sakamoto K, Minamizato T, Furukawa K, et al. (2007) BMP-2 promotes differentiation of osteoblasts and chondroblasts in Runx2-deficient cell lines. Journal of Cellular Physiology 211: 728-735 doi:10.1002/jcp.20988.
43. Pan Q, Yu Y, Chen Q, Li C, Wu H, et al. (2008) Sox9, a key transcription factor of bone morphogenetic protein-2-induced chondrogenesis, is activated through BMP pathway and a CCAAT box in the proximal promoter. J Cell Physiol 217: 228-241 doi:10.1002/jcp.21496.
44. Holleville N, Quilhac A, Bontoux M, Monsoro-Burq AH, (2003) BMP signals regulate Dlx5 during early avian skull development. Dev Biol 257: 177-189.
45. Minina E, Wenzel HM, Kreschel C, Karp S, Gaffield W, et al. (2001) BMP and Ihh/PTHrP signaling interact to coordinate chondrocyte proliferation and differentiation. Development 128: 4523-4534.
46. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L, (2007) A global double-fluorescent Cre reporter mouse. Genesis 45: 593-605 doi:10.1002/dvg.20335.
47. Nakamura E, Nguyen M-T, Mackem S, (2006) Kinetics of tamoxifen-regulated Cre activity in mice using a cartilage-specific CreER(T) to assay temporal activity windows along the proximodistal limb skeleton. Dev Dyn 235: 2603-2612 doi:10.1002/dvdy.20892.
48. Zhang SQ, Yang W, Kontaridis MI, Bivona TG, Wen G, et al. (2004) Shp2 Regulates Src Family Kinase Activity and Ras/Erk Activation by Controlling Csk Recruitment. Molecular Cell 13: 341-355 doi:10.1016/S1097-2765(04)00050-4.
49. Hayashi S, McMahon AP, (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305-318 doi:10.1006/dbio.2002.0597.
50. Gosset M, Berenbaum F, Thirion S, Jacques C, (2008) Primary culture and phenotyping of murine chondrocytes. Nature Protocols 3: 1253-1260 doi:10.1038/nprot.2008.95.
51. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111 doi:10.1093/bioinformatics/btp120.
52. Carlson M, Pages H, Aboyoun S, Falcon S, Morgan M, et al. (2012) GenomicFeatures: Tools for making and manipulating transcript centric annotations. R package version 1.8.2. Available: http://www.bioconductor.org/packages/release/bioc/html/GenomicFeatures.html.
53. Ayturk UM, Jacobsen CM, Christodoulou DC, Gorham J, Seidman JG, et al. (2013) An RNA-seq protocol to identify mRNA expression changes in mouse diaphyseal bone: applications in mice with bone property altering Lrp5 mutations. J Bone Miner Res 28: 2081-2093 doi:10.1002/jbmr.1946.
54. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140 doi:10.1093/bioinformatics/btp616.
55. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method. Methods 25: 402-408 doi:10.1006/meth.2001.1262.