CXCR4 antagonism attenuates load-induced periosteal bone formation in mice

Journal of Orthopaedic Research

Volumn 31, Issue 11, 2013, Pages 1828-1838

  Leucht, Philipp ^a   Temiyasathit, Sara ^b   Russell, Ashley ^b   Arguello, Juan F ^b   Jacobs, Christopher R ^c   Helms, Jill A ^a   Castillo, Alesha B ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^c Columbia University ^*  (United States)

Author keywords

CXCR4; mechanoadaptation; osteogenesis; SDF 1; ulnar loading

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; COMPLEMENTARY DNA; MESSENGER RNA; PLERIXAFOR; STROMAL CELL DERIVED FACTOR 1;

ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IN VITRO STUDY; MECHANICAL STIMULATION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSSIFICATION; OSTEOCYTE; OSTEOPOROSIS; PERIOSTEUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ULNA;

CXCR4; MECHANOADAPTATION; OSTEOGENESIS; SDF-1; ULNAR LOADING;

ANIMALS; CELL DIFFERENTIATION; CHEMOKINE CXCL12; HETEROCYCLIC COMPOUNDS; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; OSTEOGENESIS; RECEPTORS, CXCR4; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84884906809     PISSN: 07360266     EISSN: 1554527X     Source Type: Journal    
DOI: 10.1002/jor.22440     Document Type: Article

References (52)

1. Rubin CT, Lanyon LE,. 1985. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int 37: 411-417.
2. Rubin CT, Bain SD, McLeod KJ,. 1992. Suppression of the osteogenic response in the aging skeleton. Calcif Tissue Int 50: 306-313.
3. Smith EL, Gilligan C, McAdam M, et al. 1989. Deterring bone loss by exercise intervention in premenopausal and postmenopausal women. Calcif Tissue Int 44: 312-321.
4. Burge R, Dawson-Hughes B, Solomon DH, et al. 2007. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. J Bone Miner Res 22: 465-475.
5. Rittweger J, Simunic B, Bilancio G, et al. 2009. Bone loss in the lower leg during 35 days of bed rest is predominantly from the cortical compartment. Bone 44: 612-618.
6. Kontulainen S, Sievänen H, Kannus P, et al. 2003. Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet-sports players: a peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res 18: 352-359.
7. Pead MJ, Skerry TM, Lanyon LE,. 1988. Direct transformation from quiescence to bone formation in the adult periosteum following a single brief period of bone loading. J Bone Miner Res 3: 647-656.
8. Turner CH, Owan I, Alvey T, et al. 1998. Recruitment and proliferative responses of osteoblasts after mechanical loading in vivo determined using sustained-release bromodeoxyuridine. Bone 22: 463-469.
9. Otsuru S, Tamai K, Yamazaki T, et al. 2007. Bone marrow-derived osteoblast progenitor cells in circulating blood contribute to ectopic bone formation in mice. Biochem Biophys Res Commun 354: 453-458.
10. Pablos JL, Amara A, Bouloc A, et al. 1999. Stromal-cell derived factor is expressed by dendritic cells and endothelium in human skin. Am J Pathol 155: 1577-1586.
11. Kortesidis A, Zannettino A, Isenmann S, et al. 2005. Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood 105: 3793-3801.
12. Ratajczak MZ, Majka M, Kucia M, et al. 2003. Expression of functional CXCR4 by muscle satellite cells and secretion of SDF-1 by muscle-derived fibroblasts is associated with the presence of both muscle progenitors in bone marrow and hematopoietic stem/progenitor cells in muscles. Stem Cells 21: 363-371.
13. Hunger C, Odemis V, Engele J,. 2012. Expression and function of the SDF-1 chemokine receptors CXCR4 and CXCR7 during mouse limb muscle development and regeneration. Exp Cell Res 318: 2178-2190.
14. Sun YX, Schneider A, Jung Y, et al. 2005. Skeletal localization and neutralization of the SDF-1(CXCL12)/CXCR4 axis blocks prostate cancer metastasis and growth in osseous sites in vivo. J Bone Miner Res 20: 318-329.
15. Bosch-Marce M, Okuyama H, Wesley JB, et al. 2007. Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia. Circ Res 101: 1310-1318.
16. Ma Q, Jones D, Springer TA,. 1999. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 10: 463-471.
17. Kucia M, Jankowski K, Reca R, et al. 2004. CXCR4-SDF-1 signalling, locomotion, chemotaxis and adhesion. J Mol Histol 35: 233-245.
18. Levoye A, Balabanian K, Baleux F, et al. 2009. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 113: 6085-6093.
19. Boldajipour B, Mahabaleshwar H, Kardash E, et al. 2008. Control of chemokine-guided cell migration by ligand sequestration. Cell 132: 463-473.
20. Hosogane N, Huang Z, Rawlins BA, et al. 2010. Stromal derived factor-1 regulates bone morphogenetic protein 2-induced osteogenic differentiation of primary mesenchymal stem cells. Int J Biochem Cell Biol 42: 1132-1141.
21. Jung Y, Wang J, Schneider A, et al. 2006. Regulation of SDF-1 (CXCL12) production by osteoblasts; a possible mechanism for stem cell homing. Bone 38: 497-508.
22. Hattori K, Heissig B, Tashiro K, et al. 2001. Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood 97: 3354-3360.
23. Kitaori T, Ito H, Schwarz EM, et al. 2009. Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis Rheum 60: 813-823.
24. Toupadakis CA, Wong A, Genetos DC, et al. 2012. Long-term administration of AMD3100, an antagonist of SDF-1/CXCR4 signaling, alters fracture repair. J Orthop Res 30: 1853-1859.
25. Guan M, Yao W, Liu R, et al. 2012. Directing mesenchymal stem cells to bone to augment bone formation and increase bone mass. Nat Med 18: 456-462.
26. Bhattacharyya BJ, Banisadr G, Jung H, et al. 2008. The chemokine stromal cell-derived factor-1 regulates GABAergic inputs to neural progenitors in the postnatal dentate gyrus. J Neurosci 28: 6720-6730.
27. Lee KC, Maxwell A, Lanyon LE,. 2002. Validation of a technique for studying functional adaptation of the mouse ulna in response to mechanical loading. Bone 31: 407-412.
28. Castillo AB, Alam I, Tanaka SM, et al. 2006. Low-amplitude, broad-frequency vibration effects on cortical bone formation in mice. Bone 39: 1087-1096.
29. Robling AG, Li J, Shultz KL, et al. 2003. Evidence for a skeletal mechanosensitivity gene on mouse chromosome 4. FASEB J 17: 324-326.
30. Robling AG, Turner CH,. 2002. Mechanotransduction in bone: genetic effects on mechanosensitivity in mice. Bone 31: 562-569.
31. Robling AG, Hinant FM, Burr DB, et al. 2002. Improved bone structure and strength after long-term mechanical loading is greatest if loading is separated into short bouts. J Bone Miner Res 17: 1545-1554.
32. Albrecht UEG, Helms JA, Lin H,. 1997. Visualization of gene expression patterns by in situ hybridization. In:, Daston GP, editor. Molecular and cellular methods in developmental toxicology. Boca Raton, FL: CRC Press. p 23-48.
33. Tissir F, Wang CE, Goffinet AM,. 2004. Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development. Brain Res Dev Brain Res 149: 63-71.
34. Frangos JA, McIntire LV, Eskin SG,. 1988. Shear stress induced stimulation of mammalian cell metabolism. Biotechnol Bioeng 32: 1053-1060.
35. Jacobs CR, Yellowley CE, Davis BR, et al. 1998. Differential effect of steady versus oscillating flow on bone cells. J Biomech 31: 969-976.
36. Miyachi K, Fritzler MJ, Tan EM,. 1978. Autoantibody to a nuclear antigen in proliferating cells. J Immunol 121: 2228-2234.
37. Arnsdorf EJ, Tummala P, Kwon RY, et al. 2009. Mechanically induced osteogenic differentiation-the role of RhoA, ROCKII and cytoskeletal dynamics. J Cell Sci 122: 546-553.
38. Ponomaryov T, Peled A, Petit I, et al. 2000. Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest 106: 1331-1339.
39. Tokoyoda K, Egawa TT, Sugiyama TT, et al. 2004. Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 20: 707-718.
40. Poole KE, van Bezooijen RL, Loveridge N, et al. 2005. Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. FASEB J 19: 1842-1844.
41. Gluhak-Heinrich J, Ye L, Bonewald LF, et al. 2003. Mechanical loading stimulates dentin matrix protein 1 (DMP1) expression in osteocytes in vivo. J Bone Miner Res 18: 807-817.
42. Harris SE, Gluhak-Heinrich J, Harris MA, et al. 2007. DMP1 and MEPE expression are elevated in osteocytes after mechanical loading in vivo: theoretical role in controlling mineral quality in the perilacunar matrix. J Musculoskel Neuron Interact 7: 313-315.
43. Bonewald LF,. 2007. Osteocytes as dynamic multifunctional cells. Ann N Y Acad Sci 1116: 281-290.
44. Ehrlich PJ, Lanyon LE,. 2002. Mechanical strain and bone cell function: a review. Osteoporos Int 13: 688-700.
45. Knothe Tate ML, Knothe U,. 2000. An ex vivo model to study transport processes and fluid flow in loaded bone. J Biomech 33: 247-254.
46. Knothe Tate ML, Niederer P, Knothe U,. 1998. In vivo tracer transport through the lacunocanalicular system of rat bone in an environment devoid of mechanical loading. Bone 22: 107-117.
47. Zhu W, Liang G, Huang Z, et al. 2011. Conditional inactivation of the CXCR4 receptor in osteoprecursors reduces postnatal bone formation due to impaired osteoblast development. J Biol Chem 286: 26794-26805.
48. Ceradini DJ, Kulkarni AR, Callaghan MJ, et al. 2004. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10: 858-864.
49. Wise JK, Sumner DR, Virdi AS,. 2012. Modulation of stromal cell-derived factor-1/CXC chemokine receptor 4 axis enhances rhBMP-2-induced ectopic bone formation. Tissue Eng Part A 18: 860-869.
50. Shinohara K, Greenfield S, Pan H, et al. 2011. Stromal cell-derived factor-1 and monocyte chemotactic protein-3 improve recruitment of osteogenic cells into sites of musculoskeletal repair. J Orthop Res 29: 1064-1069.
51. Herberg S, Fulzele S, Yang N, et al. 2013. Stromal cell-derived factor-1beta potentiates bone morphogenetic protein-2-stimulated osteoinduction of genetically engineered bone marrow-derived mesenchymal stem cells in vitro. Tissue Eng Part A 19: 1-13.
52. Luan J, Cui Y, Zhang Y, et al. 2012. Effect of CXCR4 inhibitor AMD3100 on alkaline phosphatase activity and mineralization in osteoblastic MC3T3-E1 cells. Biosci Trends 6: 63-69.