Sustained epidermal growth factor receptor levels and activation by tethered ligand binding enhances osteogenic differentiation of multi-potent marrow stromal cells

Journal of Cellular Physiology

Volumn 221, Issue 2, 2009, Pages 306-317

  Platt, Manu O ^a   Roman, Arian J ^a   Wells, Alan ^b   Lauffenburger, Douglas A ^a   Griffith, Linda G ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; MITOGEN ACTIVATED PROTEIN KINASE; EPIDERMAL GROWTH FACTOR; LIGAND; MESSENGER RNA; TRANSFORMING GROWTH FACTOR ALPHA;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; COVALENT BOND; DIMERIZATION; DOWN REGULATION; ENZYME ACTIVATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERNALIZATION; LIGAND BINDING; MINERALIZATION; MULTIPOTENT STEM CELL; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STROMA CELL; BIOLOGICAL MODEL; BONE DEVELOPMENT; BONE MARROW CELL; BONE MATRIX; BONE MINERALIZATION; CELL LINE; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; PHOSPHORYLATION; SOLUBILITY; TIME;

BONE MARROW CELLS; BONE MATRIX; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CELL PROLIFERATION; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; HUMANS; LIGANDS; MODELS, BIOLOGICAL; MULTIPOTENT STEM CELLS; OSTEOGENESIS; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER; SIGNAL TRANSDUCTION; SOLUBILITY; STROMAL CELLS; TIME FACTORS; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 69949184121     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21854     Document Type: Article

References (49)

1. Chen L, Tredget EE, Wu PY, Wu Y. 2008. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS ONE 3:e1886. (Pubitemid 351943822)
2. Citri A, Yarden Y. 2006. EGF-ERBB signalling: Towards the systems level. Nat Rev Mol Cell Biol 7:505-516. (Pubitemid 44036456)
3. Citri A, Skaria KB, Yarden Y. 2003. The deaf and the dumb: The biology of ErbB-2 and ErbB-3. Exp Cell Res 284:54-65. (Pubitemid 36342255)
4. Fan VH, Tamama K, Au A, Littrell R, Richardson LB, Wright JW, Wells A, Griffith LG. 2007. Tethered epidermal growth factor provides a survival advantage to mesenchymal stem cells. Stem Cells 25:1241-1251. (Pubitemid 46684884)
5. French AR, Tadaki DK, Niyogi SK, Lauffenburger DA. 1995. Intracellular trafficking of epidermal growth factor family ligands is directly influenced by the pH sensitivity of the receptor/ligand interaction. J Biol Chem 270:4334-4340.
6. Friedenstein AJ, Piatetzky S II, Petrakova KV. 1966. Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 16:381-390.
7. Galownia NC, Kushiro K, Gong Y, Asthagiri AR. 2007. Selective desensitization of growth factor signaling by cell adhesion to fibronectin. J Biol Chem 282:21758-21766. (Pubitemid 47195779)
8. Ge C, Xiao G, Jiang D, Franceschi RT. 2007. Critical role of the extracellular signal-regulated kinase-MAPK pathway in osteoblast differentiation and skeletal development. J Cell Biol 176:709-718. (Pubitemid 46333984)
9. Harrington M, Pond-Tor S, Boney CM. 2007. Role of epidermal growth factor and ErbB2 receptors in 3T3-L1 adipogenesis. Obesity (Silver Spring) 15:563-571. (Pubitemid 46643308)
10. Harris RC, Chung E, Coffey RJ. 2003. EGF receptor ligands. Exp Cell Res 284:2-13.
11. Haugh JM. 2002. Localization of receptor-mediated signal transduction pathways: The inside story. Mol Interv 2:292-307.
12. Hendriks BS, Opresko LK, Wiley HS, Lauffenburger D. 2003a. Coregulation of epidermal growth factor receptor/human epidermal growth factor receptor 2 (HER2) levels and locations: Quantitative analysis of HER2 overexpression effects. Cancer Res 63:1130-1137. (Pubitemid 36278448)
13. Hendriks BS, Opresko LK, Wiley HS, Lauffenburger D. 2003b. Quantitative analysis of HER2-mediated effects on HER2 and epidermal growth factor receptor endocytosis: Distribution of homo- and heterodimers depends on relative HER2 levels. J Biol Chem 278:23343-23351. (Pubitemid 36830149)
14. Higuchi C, Myoui A, Hashimoto N, Kuriyama K, Yoshioka K, Yoshikawa H, Itoh K. 2002. Continuous inhibition of MAPK signaling promotes the early osteoblastic differentiation and mineralization of the extracellular matrix. J Bone Miner Res 17:1785-1794.
15. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A. 2006. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 21:737-748. (Pubitemid 43376125)
16. Huang F, Goh LK, Sorkin A. 2007. EGF receptor ubiquitination is not necessary for its internalization. Proc Natl Acad Sci USA 104:16904-16909. (Pubitemid 350210963)
17. Irvine DJ, Mayes AM, Griffith LG. 2001. Nanoscale clustering of RGD peptides at surfaces using Comb polymers. 1. Synthesis and characterization of Comb thin films. Biomacromolecules 2:85-94.
18. Iyer AK, Tran KT, Griffith L, Wells A. 2008. Cell surface restriction of EGFR by a tenascin cytotactin-encoded EGF-like repeat is preferential for motility-related signaling. J Cell Physiol 214:504-512. (Pubitemid 350309007)
19. Jaiswal RK, Jaiswal N, Bruder SP, Mbalaviele G, Marshak DR, Pittenger MF. 2000. Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J Biol Chem 275:9645-9652. (Pubitemid 30185197)
20. Joslin EJ, Opresko LK, Wells A, Wiley HS, Lauffenburger DA. 2007. EGF-receptor-mediated mammary epithelial cell migration is driven by sustained ERK signaling from autocrine stimulation. J Cell Sci 120:3688-3699. (Pubitemid 350120960)
21. Kim SM, Jung JU, Ryu JS, Jin JW, Yang HJ, Ko K, You HK, Jung KY, Choo YK. 2008. Effects of gangliosides on the differentiation of human mesenchymal stem cells into osteoblasts by modulating epidermal growth factor receptors. Biochem Biophys Res Commun 371:866-871.
22. Krampera M, Pasini A, Rigo A, Scupoli MT, Tecchio C, Malpeli G, Scarpa A, Dazzi F, Pizzolo G, Vinante F. 2005. HB-EGF/HER-1 signaling in bone marrow mesenchymal stem cells: Inducing cell expansion and reversibly preventing multilineage differentiation. Blood 106:59-66. (Pubitemid 40967175)
23. Kratchmarova I, Blagoev B, Haack-Sorensen M, Kassem M, Mann M. 2005. Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science 308:1472-1477. (Pubitemid 40791302)
24. Kuhl PR, Griffith-Cima LG. 1996. Tethered epidermal growth factor as a paradigm for growth factor-induced stimulation from the solid phase. Nat Med 2:1022-1027.
25. Kumegawa M, Hiramatsu M, Hatakeyama K, Yajima T, Kodama H, Osaki T, Kurisu K. 1983. Effects of epidermal growth factor on osteoblastic cells in vitro. Calcif Tissue Int 35:542-548.
26. Kundu AK, Khatiwala CB, Putnam AJ. 2009. Extracellular matrix remodeling, integrin expression, and downstream signaling pathways influence the osteogenic differentiation of mesenchymal stem cells on poly(lactide-co-glycolide) substrates. Tissue Eng Part A 15:273-283.
27. Morita S, Shirakata Y, Shiraishi A, Kadota Y, Hashimoto K, Higashiyama S, Ohashi Y. 2007. Human corneal epithelial cell proliferation by epiregulin and its cross-induction by other EGF family members. Mol Vis 13:2119-2128. (Pubitemid 350176249)
28. Muthuswamy SK, Gilman M, Brugge JS. 1999. Controlled dimerization of ErbB receptors provides evidence for differential signaling by homo- and heterodimers. Mol Cell Biol 19:6845-6857. (Pubitemid 29441868)
29. Okamoto T, Aoyama T, Nakayama T, Nakamata T, Hosaka T, Nishijo K, Nakamura T, Kiyono T, Toguchida J. 2002. Clonal heterogeneity in differentiation potential of immortalized human mesenchymal stem cells. Biochem Biophys Res Commun 295:354-361. (Pubitemid 34785842)
30. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147. (Pubitemid 29282067)
31. Qin L, Tamasi J, Raggatt L, Li X, Feyen JH, Lee DC, Dicicco-Bloom E, Partridge NC. 2005. Amphiregulin is a novel growth factor involved in normal bone development and in the cellular response to parathyroid hormone stimulation. J Biol Chem 280:3974-3981. (Pubitemid 40223866)
32. Reddy CC, Wells A, Lauffenburger DA. 1994. Proliferative response of fibroblasts expressing internalization-deficient epidermal growth factor (EGF) receptors is altered via differential EGF depletion effect. Biotechnol Prog 10:377-384. (Pubitemid 2129380)
33. Sato H, Kuwashima N, Sakaida T, Hatano M, Dusak JE, Fellows-Mayle WK, Papworth GD, Watkins SC, Gambotto A, Pollack IF, Okada H. 2005. Epidermal growth factor receptor-transfected bone marrow stromal cells exhibit enhanced migratory response and therapeutic potential against murine brain tumors. Cancer Gene Ther 12:757-768. (Pubitemid 41208615)
34. Satomura K, Derubeis AR, Fedarko NS, Ibaraki-O'Connor K, Kuznetsov SA, Rowe DW, Young MF, Gehron Robey P. 1998. Receptor tyrosine kinase expression in human bone marrow stromal cells. J Cell Physiol 177:426-438. (Pubitemid 28524666)
35. Schmidt MH, Furnari FB, Cavenee WK, Bogler O. 2003. Epidermal growth factor receptor signaling intensity determines intracellular protein interactions, ubiquitination, and internalization. Proc Natl Acad Sci US 100:6505-6510. (Pubitemid 36666611)
36. Sekiya I, Larson BL, Smith JR, Pochampally R, Cui JG, Prockop DJ. 2002. Expansion of human adult stem cells from bone marrow stroma: Conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 20:530-541. (Pubitemid 35463066)
37. Seth D, Shaw K, Jazayeri J, Leedman PJ. 1999. Complex post-transcriptional regulation of EGF-receptor expression by EGF and TGF-alpha in human prostate cancer cells. Br J Cancer 80:657-669. (Pubitemid 29209826)
38. Sibilia M, Wagner B, Hoebertz A, Elliott C, Marino S, Jochum W, Wagner EF. 2003. Mice humanised for the EGF receptor display hypomorphic phenotypes in skin, bone and heart. Development 130:4515-4525. (Pubitemid 37279406)
39. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S. 2005. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci USA 102:2760-2765.
40. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. 2008. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 15:209-219.
41. Tamama K, Fan VH, Griffith LG, Blair HC, Wells A. 2006. Epidermal growth factor as a candidate for ex vivo expansion of bone marrow-derived mesenchymal stem cells. Stem Cells 24:686-695. (Pubitemid 44464773)
42. Taub N, Teis D, Ebner HL, Hess MW, Huber LA. 2007. Late endosomal traffic of the epidermal growth factor receptor ensures spatial and temporal fidelity of mitogen-activated protein kinase signaling. Mol Biol Cell 18:4698-4710. (Pubitemid 350246673)
43. Vieira AV, Lamaze C, Schmid SL. 1996. Control of EGF receptor signaling by clathrinmediated endocytosis. Science 274:2086-2089. (Pubitemid 27020702)
44. Wang Y, Pennock S, Chen X, Wang Z. 2002. Endosomal signaling of epidermal growth factor receptor stimulates signal transduction pathways leading to cell survival. Mol Cell Biol 22:7279-7290.
45. Watton SJ, Downward J. 1999. Akt/PKB localisation and 3' phosphoinositide generation at sites of epithelial cell-matrix and cell-cell interaction. Curr Biol 9:433-436. (Pubitemid 29205788)
46. Wells A, Welsh JB, Lazar CS, Wiley HS, Gill GN, Rosenfeld MG. 1990. Ligand-induced transformation by a noninternalizing epidermal growth factor receptor. Science 247: 962-964. (Pubitemid 20081660)
47. Wiley HS. 2003. Trafficking of the ErbB receptors and its influence on signaling. Exp Cell Res 284:78-88.
48. Wu CJ, Chen Z, Ullrich A, Greene MI, O'Rourke DM. 2000. Inhibition of EGFR-mediated phosphoinositide-3-OH kinase (PI3-K) signaling and glioblastoma phenotype by signal-regulatory proteins (SIRPs). Oncogene 19:3999-4010.
49. Xia Z, Locklin RM, Triffitt JT. 2008. Fates and osteogenic differentiation potential of human mesenchymal stem cells in immunocompromised mice. Eur J Cell Biol 87:353-364.