Src kinases mediate VEGFR2 transactivation by the osteostatin domain of PTHrP to modulate osteoblastic function

Journal of Cellular Biochemistry

Volumn 114, Issue 6, 2013, Pages 1404-1413

  García Martín, Adela ^a   Acitores, Alicia ^b   Maycas, Marta ^a   Villanueva Peñacarrillo, María L ^b   Esbrit, Pedro ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b 28400 Madrid   (Spain)

Author keywords

Osteoblasts; Osteostatin; Src Kinases; Vascular Endothelial Growth Factor

Indexed keywords

2,3 DIHYDRO 2 OXO 3 (4,5,6,7 TETRAHYDRO 1H INDOL 2 YLMETHYLENE) 1H INDOLE 5 SULFONIC ACID DIMETHYLAMIDE; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOPROTEGERIN; OSTEOSTATIN; PARATHYROID HORMONE RELATED PROTEIN; PEPTIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; RECEPTOR BLOCKING AGENT; SU 1498; TYROSINE; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNOBLOTTING; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; RAT; TRANSACTIVATION; UPREGULATION;

3T3 CELLS; ANIMALS; CELL SURVIVAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MICE; OSTEOBLASTS; PARATHYROID HORMONE-RELATED PROTEIN; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SRC-FAMILY KINASES; TRANSCRIPTIONAL ACTIVATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

RATTUS;

EID: 84876234405     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24482     Document Type: Article

References (57)

1. Alonso V, de Gortázar AR, Ardura JA, Andrade-Zapata I, Alvarez-Arroyo MV, Esbrit P,. 2008. Parathyroid hormone-related protein (107-139) increases human osteoblastic cell survival by activation of vascular endothelial growth factor receptor-2. J Cell Physiol 217: 717-727.
2. Ardura JA, Rayego-Mateos S, Rámila D, Ruiz-Ortega M, Esbrit P,. 2010. Parathyroid hormone-related protein promotes epithelial-mesenchymal transition. J Am Soc Nephrol 21: 237-248.
3. Bellido T, Ali AA, Plotkin LI, Fu Q, Gubrij I, Roberson PK, Weinstein RS, O'Brien CA, Manolagas SC, Jilka RL,. 2003. Proteasomal degradation of Runx2 shortens parathyroid hormone-induced anti-apoptotic signaling in osteoblasts. J Biol Chem 278: 50259-50272.
4. Biscardi JS, Maa MC, Tice DA, Cox ME, Leu TH, Parsons SJ,. 1999. c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J Biol Chem 274: 8335-8343.
5. Boyce BF, Xing L,. 2008. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys 473: 139-146.
6. Bromann PA, Korkaya H, Courtneidge SA,. 2004. The interplay between Src family kinases and receptor tyrosine kinases. Oncogene 23: 7957-7968.
7. Chen HT, Tsou HK, Chang CH, Tang CH,. 2012a. Hepatocyte growth factor increases osteopontin expression in human osteoblasts through PI3K, Akt, c-Src, and AP-1 signaling pathway. PLoS ONE 7: e38378.
8. Chen D, Tian W, Li Y, Tang W, Zhang C,. 2012b. Osteoblast-specific transcription factor Osterix (Osx) and HIF-1α cooperatively regulates gene expression of vascular endothelial growth factor (VEGF). Biochem Biophys Res Commun 424: 176-181.
9. Chou MT, Wang J, Fujita DJ,. 2002. Src kinase becomes preferentially associated with the VEGFR, KDR/Flk-1, following VEGF stimulation of vascular endothelial cells. BMC Biochem 3: 32.
10. Datta NS, Abou-Samra AB,. 2009. PTH and PTHrP signaling in osteoblasts. Cell Signal 21: 1245-1254.
11. Dayanir V, Meyer RD, Lashkari K, Rahimi N,. 2001. Identification of tyrosine residues in vascular endothelial growth factor receptor-2/FLK-1 involved in activation of phosphatidylinositol 3-kinase and cell proliferation. J Biol Chem 276: 17686-17692.
12. de Castro LF, Lozano D, Dapía S, Portal-Nuñez S, Caeiro JR, Gomez-Barrena E, Esbrit P,. 2010. Role of the N- and C-terminal fragments of parathyroid hormone-related protein as putative therapies to improve bone regeneration under high glucocorticoid treatment. Tissue Eng Part A 16: 1157-1168.
13. de Castro LF, Lozano D, Portal-Núñez S, Maycas M, De la Fuente M, Caeiro JR, Esbrit P,. 2012. Comparison of the skeletal effects induced by daily administration of PTHrP (1-36) and PTHrP (107-139) to ovariectomized mice. J Cell Physiol 227: 1752-1760.
14. Deckers MM, Karperien M, van der Bent C, Yamashita T, Papapoulos SE, Löwik CW,. 2000. Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology 141: 1667-1674.
15. de Gortázar AR, Alonso V, Alvarez-Arroyo MV, Esbrit P,. 2006. Transient exposure to PTHrP (107-139) exerts anabolic effects through vascular endothelial growth factor receptor 2 in human osteoblastic cells in vitro. Calcif Tissue Int 79: 360-369.
16. de Miguel F, Fiaschi-Taesch N, Lõpez-Talavera JC, Takane KK, Massfelder T, Helwig JJ, Stewart AF,. 2001. The C-terminal region of PTHrP, in addition to the nuclear localization signal, is essential for the intracrine stimulation of proliferation in vascular smooth muscle cells. Endocrinology 142: 4096-4105.
17. Dougher M, Terman BI,. 1999. Autophosphorylation of KDR in the kinase domain is required for maximal VEGF-stimulated kinase activity and receptor internalization. Oncogene 18: 1619-1627.
18. Dougher-Vermazen M, Hulmes JD, Böhlen P, Terman BI,. 1994. Biological activity and phosphorylation sites of the bacterially expressed cytosolic domain of the KDR VEGF-receptor. Biochem Biophys Res Commun 205: 728-738.
19. Esbrit P, Alvarez-Arroyo MV, de Miguel F, Martín O, Martínez ME, Caramelo C,. 2000. C-terminal parathyroid hormone-related protein increases vascular endothelial growth factor in human osteoblastic cells. J Am Soc Nephrol 11: 1085-1092.
20. Fujita Y, Yoshizumi M, Izawa Y, Ali N, Ohnishi H, Kanematsu Y, Ishizawa K, Tsuchiya K, Tamaki T,. 2006. Transactivation of fetal liver kinase-1/kinase-insert domain-containing receptor by lysophosphatidylcholine induces vascular endothelial cell proliferation. Endocrinology 147: 1377-1385.
21. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N,. 1998. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273: 30336-30343.
22. Hobbs SS, Goettel JA, Liang D, Yan F, Edelblum KL, Frey MR, Mullane MT, Polk DB,. 2011. TNF transactivation of EGFR stimulates cytoprotective COX-2 expression in gastrointestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 301: G220-G229.
23. Jin ZG, Ueba H, Tanimoto T, Lungu AO, Frame MD, Berk BC,. 2003. Ligand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ Res 93: 354-363.
24. 2 receptors by extracellular ATP is involved in osteoblastic cell proliferation. Arch Biochem Biophys 513: 144-152.
25. Kendall RL, Rutledge RZ, Mao X, Tebben AJ, Hungate RW, Thomas KA,. 1999. Vascular endothelial growth factor receptor KDR tyrosine kinase activity is increased by autophosphorylation of two activation loop tyrosine residues. J Biol Chem 274: 6453-6460.
26. Koch S, Claesson-Welsh L,. 2012. Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harb Perspect Med 2: a006502.
27. Kroll J, Waltenberger J,. 1997. The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells. J Biol Chem 272: 32521-32527.
28. Lausson S, Cressent M,. 2011. Signal transduction pathways mediating the effect of adrenomedullin on osteoblast survival. J Cell Biochem 112: 3807-3815.
29. Liu J, Agarwal S,. 2010. Mechanical signals activate vascular endothelial growth factor receptor-2 to upregulate endothelial cell proliferation during inflammation. J Immunol 185: 1215-1221.
30. Lozano D, Manzano M, Doadrio JC, Salinas AJ, Vallet-Regí M, Gõmez-Barrena E, Esbrit P,. 2010. Osteostatin-loaded bioceramics stimulate osteoblastic growth and differentiation. Acta Biomater 6: 797-803.
31. Lozano D, Fernández-de-Castro L, Portal-Núñez S, Lõpez-Herradõn A, Dapía S, Gõmez-Barrena E, Esbrit P,. 2011. The C-terminal fragment of parathyroid hormone-related peptide promotes bone formation in diabetic mice with low turnover osteopenia. Br J Pharmacol 162: 1424-1438.
32. Lozano D, Trejo CG, Gõmez-Barrena E, Manzano M, Doadrio JC, Salinas AJ, Vallet-Regí M, García-Honduvilla N, Esbrit P, Buján J,. 2012a. Osteostatin-loaded onto mesoporous ceramics improves the early phase of bone regeneration in a rabbit osteopenia model. Acta Biomater 8: 2317-2323.
33. Lozano D, Feito MJ, Portal-Núñez S, Lozano RM, Matesanz MC, Serrano MC, Vallet-Regí M, Portolés MT, Esbrit P,. 2012b. Osteostatin improves the osteogenic activity of fibroblast growth factor-2 immobilized on Si-doped hydroxyapatite in osteoblastic cells. Acta Biomater 8: 2770-2777.
34. Marzia M, Sims NA, Voit S, Migliaccio S, Taranta A, Bernardini S, Faraggiana T, Yoneda T, Mundy GR, Boyce BF, Baron R, Teti A,. Decreased c-Src expression enhances osteoblast differentiation and bone formation. J Cell Biol 151: 311-320.
35. Matsumoto T, Claesson-Welsh L,. 2001. VEGF receptor signal transduction. Sci STKE 112: re21.
36. Matsumoto T, Mugishima H,. 2006. Signal transduction via vascular endothelial growth factor (VEGF) receptors and their roles in atherogenesis. J Atheroscler Thromb 13: 130-135.
37. Miao D, Su H, He B, Gao J, Xia Q, Zhu M, Gu Z, Goltzman D, Karaplis AC,. 2008. Severe growth retardation and early lethality in mice lacking the nuclear localization sequence and C-terminus of PTH-related protein. Proc Natl Acad Sci USA 105: 20309-20311.
38. Pedram A, Razandi M, Levin ER,. 1998. Extracellular signal-regulated protein kinase/Jun kinase cross-talk underlies vascular endothelial cell growth factor-induced endothelial cell proliferation. J Biol Chem 273: 26722-26728.
39. Peng H, Usas A, Olshanski A, Ho AM, Gearhart B, Cooper GM, Huard J,. 2005. VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulation of angiogenesis. J Bone Miner Res 20: 2017-2027.
40. Petreaca ML, Yao M, Liu Y, DeFea K, Martins-Green M,. 2007. Transactivation of vascular endothelial growth factor receptor-2 (VEGFR2) by interleukin-8 (IL-8/CXCL8) is required for IL-8/CXCL8-induced endothelial permeability. Mol Biol Cell 18: 5014-5023.
41. Portal-Núñez S, Lozano D, Esbrit P,. 2012. Role of angiogenesis in bone formation. Histol Histopathol 27: 559-566.
42. Roskoski R, Jr., 2004. Src protein-tyrosine kinase structure and regulation. Biochem Biophys Res Commun 324: 1155-1164.
43. Samee M, Kasugai S, Kondo H, Ohya K, Shimokawa H, Kuroda S,. 2008. Bone morphogenetic protein-2 (BMP-2) and vascular endothelial growth factor (VEGF) transfection to human periosteal cells enhances osteoblast differentiation and bone formation. J Pharmacol Sci 108: 18-31.
44. Santos SC, Dias S,. 2004. Internal and external autocrine VEGF/KDR loops regulate survival of subsets of acute leukemia through distinct signaling pathways. Blood 103: 3883-3889.
45. Santos SC, Miguel C, Domingues I, Calado A, Zhu Z, Wu Y, Dias S,. 2007. VEGF and VEGFR-2 (KDR) internalization is required for endothelial recovery during wound healing. Exp Cell Res 313: 1561-1574.
46. Schipani E, Maes C, Carmeliet G, Semenza GL,. 2009. Regulation of osteogenesis-angiogenesis coupling by HIFs and VEGF. J Bone Miner Res 24: 1347-1353.
47. Takahashi T, Yamaguchi S, Chida K, Shibuya M,. 2001. A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells. EMBO J 20: 2768-2778.
48. Tang W, Yang F, Li Y, de Crombrugghe B, Jiao H, Xiao G, Zhang C,. 2012. Transcriptional regulation of vascular endothelial growth factor (VEGF) by osteoblast-specific transcription factor osterix (Osx) in osteoblasts. J Biol Chem 287: 1671-1678.
49. Tanimoto T, Jin ZG, Berk BC,. 2002. Transactivation of vascular endothelial growth factor (VEGF) receptor Flk-1/KDR is involved in sphingosine 1-phosphate-stimulated phosphorylation of Akt and endothelial nitric-oxide synthase (eNOS). J Biol Chem 277: 42997-43001.
50. Thomas SM, Brugge JS,. 1997. Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13: 513-609.
51. Toribio RE, Brown HA, Novince CM, Marlow B, Hernon K, Lanigan LG, Hildreth BE III, Werbeck JL, Shu ST, Lorch G, Carlton M, Foley J, Boyaka P, McCauley LK, Rosol TJ,. 2010. The midregion, nuclear localization sequence, and C terminus of PTHrP regulate skeletal development, hematopoiesis, and survival in mice. FASEB J 24: 1947-1957.
52. Trejo CG, Lozano D, Manzano M, Doadrio JC, Salinas AJ, Dapía S, Gõmez-Barrena E, Vallet-Regí M, García-Honduvilla N, Buján J, Esbrit P,. 2010. The osteoinductive properties of mesoporous silicate coated with osteostatin in a rabbit femur cavity defect model. Biomaterials 31: 8564-8573.
53. 2+ through a receptor different from the type 1 PTH/PTHrP receptor in osteoblastic osteosarcoma UMR 106 cells. Endocrinology 142: 2752-2759.
54. Zachary I, Gliki G,. 2001. Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family. Cardiovasc Res 49: 568-581.
55. Zeng H, Sanyal S, Mukhopadhyay D,. 2001. Tyrosine residues 951 and 1059 of vascular endothelial growth factor receptor-2 (KDR) are essential for vascular permeability factor/vascular endothelial growth factor-induced endothelium migration and proliferation, respectively. J Biol Chem 276: 32714-32719.
56. Zhang R, Xu Y, Ekman N, Wu Z, Wu J, Alitalo K, Min W,. 2003. Etk/Bmx transactivates vascular endothelial growth factor 2 and recruits phosphatidylinositol 3-kinase to mediate the tumor necrosis factor-induced angiogenic pathway. J Biol Chem 278: 51267-51276.
57. Zilberberg L, Shinkaruk S, Lequin O, Rousseau B, Hagedorn M, Costa F, Caronzolo D, Balke M, Canron X, Convert O, Lain G, Gionnet K, Gonçalves M, Bayle M, Bello L, Chassaing G, Deleris G, Bikfalvi A,. 2003. Structure and inhibitory effects on angiogenesis and tumor development of a new vascular endothelial growth inhibitor. J Biol Chem 278: 35564-35573.