Amphiregulin-EGFR Signaling Mediates the Migration of Bone Marrow Mesenchymal Progenitors toward PTH-Stimulated Osteoblasts and Osteocytes

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Zhu, Ji ^a   Siclari, Valerie A ^a   Liu, Fei ^a,b   Spatz, Jordan M ^c   Chandra, Abhishek ^a   Divieti Pajevic, Paola ^c   Qin, Ling ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIREGULIN; CYCLIC AMP; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUTRALIZING ANTIBODY; PARATHYROID HORMONE RECEPTOR; PARATHYROID HORMONE[1-34]; PROTEIN KINASE B; SMALL INTERFERING RNA;

ARTICLE; BONE MARROW; CELL MIGRATION; CELL STIMULATION; CHEMOTAXIS; CONTROLLED STUDY; DRUG MECHANISM; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; METABOLIC INHIBITION; OSSIFICATION; OSTEOBLAST; OSTEOCYTE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; BONE DENSITY; BONE MARROW; CELL MOVEMENT; CELL PROLIFERATION; CHEMOTAXIS; CULTURE MEDIA, CONDITIONED; FEMALE; FLOW CYTOMETRY; GLYCOPROTEINS; HUMANS; IMMUNOENZYME TECHNIQUES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, KNOCKOUT; OSTEOBLASTS; OSTEOCYTES; OSTEOGENESIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PARATHYROID HORMONE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, PARATHYROID HORMONE, TYPE 1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84871773355     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050099     Document Type: Article

References (50)

1. Dempster DW, Cosman F, Parisien M, Shen V, Lindsay R, (1993) Anabolic actions of parathyroid hormone on bone. Endocr Rev 14: 690-709.
2. Tam CS, Heersche JN, Murray TM, Parsons JA, (1982) Parathyroid hormone stimulates the bone apposition rate independently of its resorptive action: differential effects of intermittent and continuous administration. Endocrinology 110: 506-512.
3. Rouleau MF, Mitchell J, Goltzman D, (1988) In vivo distribution of parathyroid hormone receptors in bone: evidence that a predominant osseous target cell is not the mature osteoblast. Endocrinology 123: 187-191.
4. Fermor B, Skerry TM, (1995) PTH/PTHrP receptor expression on osteoblasts and osteocytes but not resorbing bone surfaces in growing rats. J Bone Miner Res 10: 1935-1943.
5. Qin L, Raggatt LJ, Partridge NC, (2004) Parathyroid hormone: a double-edged sword for bone metabolism. Trends Endocrinol Metab 15: 60-65.
6. Qin L, Qiu P, Wang L, Li X, Swarthout JT, et al. (2003) Gene expression profiles and transcription factors involved in parathyroid hormone signaling in osteoblasts revealed by microarray and bioinformatics. J Biol Chem 278: 19723-19731.
7. Li X, Liu H, Qin L, Tamasi J, Bergenstock M, et al. (2007) Determination of dual effects of parathyroid hormone on skeletal gene expression in vivo by microarray and network analysis. J Biol Chem 282: 33086-33097.
8. Jilka RL, (2007) Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone 40: 1434-1446.
9. Knopp E, Troiano N, Bouxsein M, Sun BH, Lostritto K, et al. (2005) The effect of aging on the skeletal response to intermittent treatment with parathyroid hormone. Endocrinology 146: 1983-1990.
10. Sakai A, Sakata T, Ikeda S, Uchida S, Okazaki R, et al. (1999) Intermittent administration of human parathyroid Hormone(1-34) prevents immobilization-related bone loss by regulating bone marrow capacity for bone cells in ddY mice. J Bone Miner Res 14: 1691-1699.
11. Kostenuik PJ, Harris J, Halloran BP, Turner RT, Morey-Holton ER, et al. (1999) Skeletal unloading causes resistance of osteoprogenitor cells to parathyroid hormone and to insulin-like growth factor-I. J Bone Miner Res 14: 21-31.
12. Nishida S, Yamaguchi A, Tanizawa T, Endo N, Mashiba T, et al. (1994) Increased bone formation by intermittent parathyroid hormone administration is due to the stimulation of proliferation and differentiation of osteoprogenitor cells in bone marrow. Bone 15: 717-723.
13. Wang Y, Nishida S, Boudignon BM, Burghardt A, Elalieh HZ, et al. (2007) IGF-I receptor is required for the anabolic actions of parathyroid hormone on bone. J Bone Miner Res 22: 1329-1337.
14. Davies J, Chambers TJ, (2004) Parathyroid hormone activates adhesion in bone marrow stromal precursor cells. J Endocrinol 180: 505-513.
15. Bianco P, (2011) Back to the future: Moving beyond "mesenchymal stem cells". J Cell Biochem 112: 1713-1721.
16. da Silva Meirelles L, Caplan AI, Nardi NB, (2008) In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26: 2287-2299.
17. Schipani E, Kronenberg HM (2009) Adult mesenchymal stem cells. StemBook. Cambridge: Harvard Stem Cell Institute.
18. Wu X, Pang L, Lei W, Lu W, Li J, et al. (2010) Inhibition of Sca-1-positive skeletal stem cell recruitment by alendronate blunts the anabolic effects of parathyroid hormone on bone remodeling. Cell Stem Cell 7: 571-580.
19. Citri A, Yarden Y, (2006) EGF-ERBB signalling: towards the systems level. Nat Rev Mol Cell Biol 7: 505-516.
20. Schneider MR, Sibilia M, Erben RG, (2009) The EGFR network in bone biology and pathology. Trends Endocrinol Metab 20: 517-524.
21. Qin L, Tamasi J, Raggatt L, Li X, Feyen JH, et al. (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.
22. Bonewald LF, (2011) The amazing osteocyte. J Bone Miner Res 26: 229-238.
23. Zhu J, Shimizu E, Zhang X, Partridge NC, Qin L, (2011) EGFR signaling suppresses osteoblast differentiation and inhibits expression of master osteoblastic transcription factors Runx2 and Osterix. J Cell Biochem 112: 1749-1760.
24. Zhang X, Tamasi J, Lu X, Zhu J, Chen H, et al. (2011) Epidermal growth factor receptor plays an anabolic role in bone metabolism in vivo. J Bone Miner Res 26: 1022-1034.
25. Caplan AI, (2009) Why are MSCs therapeutic? New data: new insight. J Pathol 217: 318-324.
26. Kalajzic I, Staal A, Yang WP, Wu Y, Johnson SE, et al. (2005) Expression profile of osteoblast lineage at defined stages of differentiation. J Biol Chem 280: 24618-24626.
27. Shinoda Y, Kawaguchi H, Higashikawa A, Hirata M, Miura T, et al. (2010) Mechanisms underlying catabolic and anabolic functions of parathyroid hormone on bone by combination of culture systems of mouse cells. J Cell Biochem 109: 755-763.
28. Barr S, Thomson S, Buck E, Russo S, Petti F, et al. (2008) Bypassing cellular EGF receptor dependence through epithelial-to-mesenchymal-like transitions. Clin Exp Metastasis 25: 685-693.
29. Ryan MA, Nattamai KJ, Xing E, Schleimer D, Daria D, et al. (2010) Pharmacological inhibition of EGFR signaling enhances G-CSF-induced hematopoietic stem cell mobilization. Nat Med 16: 1141-1146.
30. Krampera M, Pasini A, Rigo A, Scupoli MT, Tecchio C, et al. (2005) HB-EGF/HER-1 signaling in bone marrow mesenchymal stem cells: inducing cell expansion and reversibly preventing multilineage differentiation. Blood 106: 59-66.
31. 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.
32. Reiss K, Saftig P, (2009) The "a disintegrin and metalloprotease" (ADAM) family of sheddases: physiological and cellular functions. Semin Cell Dev Biol 20: 126-137.
33. Sanderson MP, Dempsey PJ, Dunbar AJ, (2006) Control of ErbB signaling through metalloprotease mediated ectodomain shedding of EGF-like factors. Growth Factors 24: 121-136.
34. Kalajzic I, Kalajzic Z, Kaliterna M, Gronowicz G, Clark SH, et al. (2002) Use of type I collagen green fluorescent protein transgenes to identify subpopulations of cells at different stages of the osteoblast lineage. J Bone Miner Res 17: 15-25.
35. Liu F, Woitge HW, Braut A, Kronenberg MS, Lichtler AC, et al. (2004) Expression and activity of osteoblast-targeted Cre recombinase transgenes in murine skeletal tissues. Int J Dev Biol 48: 645-653.
36. Lee D, Cross SH, Strunk KE, Morgan JE, Bailey CL, et al. (2004) Wa5 is a novel ENU-induced antimorphic allele of the epidermal growth factor receptor. Mamm Genome 15: 525-536.
37. Schneider MR, Mayer-Roenne B, Dahlhoff M, Proell V, Weber K, et al. (2009) High cortical bone mass phenotype in betacellulin transgenic mice is EGFR dependent. J Bone Miner Res 24: 455-467.
38. Schneider MR, Dahlhoff M, Andrukhova O, Grill J, Glosmann M, et al. (2012) Normal epidermal growth factor receptor signaling is dispensable for bone anabolic effects of parathyroid hormone. Bone 50: 237-244.
39. Compston JE, (2007) Skeletal actions of intermittent parathyroid hormone: effects on bone remodelling and structure. Bone 40: 1447-1452.
40. Gallacher SJ, Dixon T, (2010) Impact of treatments for postmenopausal osteoporosis (bisphosphonates, parathyroid hormone, strontium ranelate, and denosumab) on bone quality: a systematic review. Calcif Tissue Int 87: 469-484.
41. Prisby R, Guignandon A, Vanden-Bossche A, Mac-Way F, Linossier MT, et al. (2011) Intermittent PTH(1-84) is osteoanabolic but not osteoangiogenic and relocates bone marrow blood vessels closer to bone-forming sites. J Bone Miner Res 26: 2583-2596.
42. Lee K, Deeds JD, Chiba S, Un-No M, Bond AT, et al. (1994) Parathyroid hormone induces sequential c-fos expression in bone cells in vivo: in situ localization of its receptor and c-fos messenger ribonucleic acids. Endocrinology 134: 441-450.
43. Powell WF Jr, Barry KJ, Tulum I, Kobayashi T, Harris SE, et al. (2011) Targeted ablation of the PTH/PTHrP receptor in osteocytes impairs bone structure and homeostatic calcemic responses. J Endocrinol 209: 21-32.
44. Rhee Y, Allen MR, Condon K, Lezcano V, Ronda AC, et al. (1035) PTH receptor signaling in osteocytes governs periosteal bone formation and intracortical remodeling. J Bone Miner Res 26: 1035-1046.
45. Kramer I, Keller H, Leupin O, Kneissel M, (2010) Does osteocytic SOST suppression mediate PTH bone anabolism? Trends Endocrinol Metab 21: 237-244.
46. Yamaoka T, Frey MR, Dise RS, Bernard JK, Polk DB, (2011) Specific epidermal growth factor receptor autophosphorylation sites promote mouse colon epithelial cell chemotaxis and restitution. Am J Physiol Gastrointest Liver Physiol 301: G368-376.
47. Liu Y, Sun R, Wan W, Wang J, Oppenheim JJ, et al. (2007) The involvement of lipid rafts in epidermal growth factor-induced chemotaxis of breast cancer cells. Mol Membr Biol 24: 91-101.
48. Wu J, Zhang B, Wu M, Li H, Niu R, et al. (2010) Screening of a PKC zeta-specific kinase inhibitor PKCzI257.3 which inhibits EGF-induced breast cancer cell chemotaxis. Invest New Drugs 28: 268-275.
49. Frey MR, Golovin A, Polk DB, (2004) Epidermal growth factor-stimulated intestinal epithelial cell migration requires Src family kinase-dependent p38 MAPK signaling. J Biol Chem 279: 44513-44521.
50. Polk DB, (1998) Epidermal growth factor receptor-stimulated intestinal epithelial cell migration requires phospholipase C activity. Gastroenterology 114: 493-502.