Oxytocin controls differentiation of human mesenchymal stem cells and reverses osteoporosis

Stem Cells

Volumn 26, Issue 9, 2008, Pages 2399-2407

  Elabd, Christian ^a   Basillais, Armelle ^b   Beaupied, Hélene ^b   Breuil, Véronique ^a,c   Wagner, Nicole ^b   Scheideler, Marcel ^d   Zaragosi, Laure Emmanuelle ^a   Massiéra, Florence ^a   Lemichez, Emmanuel ^b   Trajanoski, Zlatko ^b   Carle, Georges ^a   Euller Ziegler, Liana ^c   Ailhaud, Gérard ^a   Benhamou, Claude Laurent ^b   Dani, Christian ^a   Amri, Ez Zoubir ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b INSERM   (France)

^c CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

^d GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Adipocyte; Differentiation; Mesenchymal stem cells; Osteoblast; Osteoporosis; Oxytocin

Indexed keywords

CARBETOCIN; OXYTOCIN; OXYTOCIN RECEPTOR;

ADIPOCYTE; ADIPOGENESIS; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; C57BL 6 MOUSE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; GENE LINKAGE DISEQUILIBRIUM; HEMATOPOIETIC STEM CELL; HUMAN; MALE; MESENCHYMAL STEM CELL; MOUSE; MULTIPOTENT ADIPOSE DERIVED STEM CELL; NONHUMAN; OBESITY; OSTEOBLAST; OSTEOLYSIS; OSTEOPOROSIS; OVARIECTOMY; OXYTOCIN BLOOD LEVEL; PRESCHOOL CHILD; RAT; SHAM PROCEDURE; STEM CELL; TRANSCRIPTOMICS; WISTAR RAT;

ADIPOGENESIS; AGED; AGED, 80 AND OVER; ANIMALS; BONE MARROW CELLS; CELLS, CULTURED; CHILD, PRESCHOOL; FEMALE; HUMANS; MALE; MESENCHYMAL STEM CELLS; MICE; MIDDLE AGED; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; OSTEOPOROSIS; OSTEOPOROSIS, POSTMENOPAUSAL; OVARIECTOMY; OXYTOCIN; RATS; RECEPTORS, OXYTOCIN;

MUS; RATTUS;

EID: 55049136163     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2008-0127     Document Type: Article

References (78)

1. Keen R. Osteoporosis: strategies for prevention and management. Best Pract Res Clin Rheumatol 2007;21:109-122.
2. Delmas PD, Fraser M. Strong bones in later life: luxury or necessity? Bull World Health Organ 1999;77:416-422.
3. Karsenty G, Wagner EF. Reaching a genetic and molecular understanding of skeletal development. Dev Cell 2002;2:389-406.
4. Seeman E, Delmas PD. Bone quality - the material and structural basis of bone strength and fragility. N Engl J Med 2006;354:2250-2261.
5. Rodan GA, Martin TJ. Therapeutic approaches to bone diseases. Science 2000;289:1508-1514.
6. Teitelbaum SL. Bone resorption by osteoclasts. Science 2000;289:1504-1508.
7. Rosen CJ, Bouxsein ML. Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2006;2:35-43.
8. Rodriguez AM, Elabd C, Delteil F et al. Adipocyte differentiation of multipotent cells established from human adipose tissue. Biochem Biophys Res Commun 2004;315:255-263.
9. Rodriguez AM, Pisani D, Dechesne CA et al. Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp Med 2005;201:1397-1405.
10. Zaragosi LE, Ailhaud G, Dani C. Autocrine fibroblast growth factor 2 signaling is critical for self-renewal of human multipotent adipose-derived stem cells. STEM CELLS 2006;24:2412-2419.
11. Elabd C, Chiellini C, Massoudi A et al. Human adipose tissue-derived multipotent stem cells differentiate in vitro and in vivo into osteocyte-ike cells. Biochem Biophys Res Commun 2007;361:342-348.
12. Nuttall ME, Gimble JM. Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications. Curr Opin Pharmacol 2004;4:290-294.
13. Ahdjoudj S, Fromigue O, Marie PJ. Plasticity and regulation of human bone marrow stromal osteoprogenitor cells: potential implication in the treatment of age-related bone loss. Histol Histopathol 2004;19:151-157.
14. Kulterer B, Friedl G, Jandrositz A et al. Gene expression profiling of human mesenchymal stem cells derived from bone marrow during expansion and osteoblast differentiation. Bmc Genomics 2007;8:70.
15. Boland D, Goren HJ. Binding and structural properties of oxytocin receptors in isolated rat epididymal adipocytes. Regul Pept 1987;18:7-18.
16. Copland JA, Ives KL, Simmons DJ et al. Functional oxytocin receptors discovered in human osteoblasts. Endocrinology 1999;140:4371-4374.
17. Zingg HH, Laporte SA. The oxytocin receptor. Trends Endocrinol Metab 2003;14:222-227.
18. Russell JA, Leng G, Douglas AJ. The magnocellular oxytocin system, the fount of maternity: adaptations in pregnancy. Front Neuroendocrinol 2003;24:27-61.
19. Neumann ID. Oxytocin: the neuropeptide of love reveals some of its secrets. Cell Metab 2007;5:231-233.
20. Kosfeld M, Heinrichs M, Zak PJ et al. Oxytocin increases trust in humans. Nature 2005;435:673-676.
21. Kirsch P, Esslinger C, Chen Q et al. Oxytocin modulates neural circuitry for social cognition and fear in humans. J Neurosci 2005;25:11489-11493.
22. López FJ. New approaches to the treatment of osteoporosis. Curr Opin Chem Biol 2000;4:383-393.
23. Petersson M, Lagumdzija A, Stark A et al. Oxytocin stimulates proliferation of human osteoblast-like cells. Peptides 2002;23:1121-1126.
24. Elabd SK, Sabry I, Hassan WB et al. Possible neuroendocrine role for oxytocin in bone remodeling. Endocr Regul 2007;41:131-141.
25. Négrel R, Grimaldi P, Ailhaud G. Establishment of preadipocyte clonal line from epididymal fat pad of ob/ob mouse that responds to insulin and to lipolytic hormones. Proc Natl Acad Sci U S A 1978;75:6054-6058.
26. 3 induce alkaline phosphatase activity in osteoblastic cells derived from newborn mouse calvaria. J Biochem 1983;94:1127-1132.
27. Halvorsen YD, Franklin D, Bond AL et al. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 2001;7:729-741.
28. Doye A, Mettouchi A, Bossis G et al. CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 2002;111:553-564.
29. Ren XD, Kiosses WB, Schwartz MA. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 1999;18:578-585.
30. Petersson M, Eklund M, Uvnas-Moberg K. Oxytocin decreases corticosterone and nociception and increases motor activity in OVX rats. Maturitas 2005;51:426-433.
31. Petersson M, Diaz-Cabiale Z, Angel Narvaez J et al. Oxytocin increases the density of high affinity alpha(2)-adrenoceptors within the hypothalamus, the amygdala and the nucleus of the solitary tract in ovariectomized rats. Brain Res 2005;1049:234-239.
32. Wagner N, Wagner KD, Theres H et al. Coronary vessel development requires activation of the TrkB neurotrophin receptor by the Wilms' tumor transcription factor Wt1. Genes Dev 2005;19:2631-2642.
33. Bonnet N, Laroche N, Beaupied H et al. Doping dose of salbutamol and exercise training: impact on the skeleton of ovariectomized rats. J Appl Physiol 2007;103:524-533.
34. Bonnet N, Bernard P, Beaupied H et al. Various effects of antidepressant drugs on bone microarchitectecture, mechanical properties and bone remodeling. Toxicol Appl Pharmacol 2007;221:111-118.
35. Di Masso RJ, Font MT, Capozza RF et al. Long-bone biomechanics in mice selected for body conformation. Bone 1997;20:539-545.
36. Turner CH, Burr DB. Basic biomechanical measurements of bone: a tutorial. Bone 1993;14:595-608.
37. Hunter DJ, Schulz P, Wassenaar W. Effect of carbetocin, a long-acting oxytocin analog on the postpartum uterus. Clin Pharmacol Ther 1992;52:60-67.
38. Tahara M, Morishige K, Sawada K et al. RhoA/Rho-kinase cascade is involved in oxytocin-induced rat uterine contraction. Endocrinology 2002;143:920-929.
39. Strakova Z, Copland JA, Lolait SJ et al. ERK2 mediates oxytocin-stimulated PGE2 synthesis. Am J Physiol 1998;274:E634-641.
40. McBeath R, Pirone DM, Nelson CM et al. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004;6:483-495.
41. Wang FS, Wang CJ, Sheen-Chen SM et al. Superoxide mediates shock wave induction of ERK-dependent osteogenic transcription factor (CBFA1) and mesenchymal cell differentiation toward osteoprogenitors. J Biol Chem 2002;277:10931-10937.
42. Reginato MJ, Krakow SL, Bailey ST et al. Prostaglandins promote and block adipogenesis through opposing effects on peroxisome proliferator-activated receptor gamma. J Biol Chem 1998;273:1855-1858.
43. Wronski TJ, Lowry PL, Walsh CC et al. Skeletal alterations in ovariectomized rats. Calcif Tissue Int 1985;37:324-328.
44. Jansson JO, Moverare-Skrtic S, Berndtsson A et al. Leukemia inhibitory factor reduces body fat mass in ovariectomized mice. Eur J Endocrinol 2006;154:349-354.
45. Yeung DK, Griffith JF, Antonio GE et al. Osteoporosis is associated with increased marrow fat content and decreased marrow fat unsaturation: a proton MR spectroscopy study. J Magn Reson Imaging 2005;22:279-285.
46. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. World Health Organ Tech Rep Ser 1994;843:1-129.
47. De Ugarte DA, Morizono K, Elbarbary A et al. Comparison of multilineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 2003;174:101-109.
48. Noël D, Caton D, Roche S et al. Cell specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Exp Cell Res 2008;314:1575-1584.
49. Sakaguchi Y, Sekiya I, Yagishita K et al. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 2005;52:2521-2529.
50. Gronthos S, Franklin DM, Leddy HA et al. Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 2001;189:54-63.
51. Petersson M. Opposite effects of oxytocin on proliferation of osteosarcoma cell lines. Regul Pept 2008 (in press).
52. Hata K, Nishimura R, Ueda M et al. A CCAAT/enhancer binding protein beta isoform, liver-enriched inhibitory protein, regulates commitment of osteoblasts and adipocytes. Mol Cell Biol 2005;25:1971-1979.
53. Richard S, Zingg HH. The human oxytocin gene promoter is regulated by estrogens. J Biol Chem 1990;265:6098-6103.
54. Richter ON, Kubler K, Schmolling J et al. Oxytocin receptor gene expression of estrogen-stimulated human myometrium in extracorporeally perfused non-pregnant uteri. Mol Hum Reprod 2004;10:339-346.
55. Abdallah BM, Haack-Sorensen M, Fink T et al. Inhibition of osteoblast differentiation but not adipocyte differentiation of mesenchymal stem cells by sera obtained from aged females. Bone 2006;39:181-188.
56. Stringer B, Waddington R, Sloan A et al. Serum from Postmenopausal Women Directs Differentiation of Human Clonal Osteoprogenitor Cells from an Osteoblastic toward an Adipocytic Phenotype. Calcif Tissue Int 2007;80:233-243.
57. Nishimori K, Young LJ, Guo Q et al. Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc Natl Acad Sci U S A 1996;93:11699-11704.
58. Ferguson JN, Young LJ, Hearn EF et al. Social amnesia in mice lacking the oxytocin gene. Nat Genet 2000;25:284-288.
59. Takayanagi Y, Yoshida M, Bielsky IF et al. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci U S A 2005;102:16096-16101.
60. Jee WS, Ma YF. The in vivo anabolic actions of prostaglandins in bone. Bone 1997;21:297-304.
61. Aguirre JI, Leal ME, Rivera MF et al. Effects of basic fibroblast growth factor and a prostaglandin E2 receptor subtype 4 agonist on osteoblastogenesis and adipogenesis in aged ovariectomized rats. J Bone Miner Res 2007;22:877-888.
62. Tsuboi H, Sugimoto Y, Kainoh T et al. Prostanoid EP4 receptor is involved in suppression of 3T3-L1 adipocyte differentiation. Biochem Biophys Res Commun 2004;322:1066-1072.
63. Colucci S, Colaianni G, Mori G et al. Human osteoclasts express oxytocin receptor. Biochem Biophys Res Commun 2002;297:442-445.
64. Levasseur R, Legrand E, Chappard D et al. Central control of bone mass: potential therapeutic implications. Joint Bone Spine 2005;72:474-476.
65. Takeda S. Central control of bone remodeling. Biochem Biophys Res Commun 2005;328:697-699.
66. Sun L, Peng Y, Sharrow AC et al. FSH directly regulates bone mass. Cell 2006;125:247-260.
67. Yeh JK, Chen MM, Aloia JF. Ovariectomy-induced high turnover in cortical bone is dependent on pituitary hormone in rats. Bone 1996;18:443-450.
68. Yeh JK, Chen MM, Aloia JF. Effects of 17 beta-estradiol administration on cortical and cancellous bone of ovariectomized rats with and without hypophysectomy. Bone 1997;20:413-420.
69. Seibel MJ, Dunstan CR, Zhou H et al. Sex steroids, not FSH, influence bone mass. Cell 2006;127:1079; author reply 1080-1071.
70. Mundy G, Garrett R, Harris S et al. Stimulation of bone formation in vitro and in rodents by statins. Science 1999;286:1946-1949.
71. Simic P, Culej JB, Orlic I et al. Systemically administered bone morphogenetic protein-6 restores bone in aged ovariectomized rats by increasing bone formation and suppressing bone resorption. J Biol Chem 2006;281:25509- 25521.
72. Kasukawa Y, Miyakoshi N, Srivastava AK et al. The selective cyclooxygenase-2 inhibitor celecoxib reduces bone resorption, but not bone formation, in ovariectomized mice in vivo. Tohoku J Exp Med 2007;211:275-283.
73. Sambrook P, Cooper C. Osteoporosis. Lancet 2006;367:2010-2018.
74. McCormick RK. Osteoporosis: integrating biomarkers and other diagnostic correlates into the management of bone fragility. Altern Med Rev 2007;12:113-145.
75. Rizzoli R, Burlet N, Cahall D et al. Osteonecrosis of the jaw and bisphosphonate treatment for osteoporosis. Bone 2008;42:841-847.
76. Graham DY, Malaty HM. Alendronate gastric ulcers. Aliment Pharmacol Ther 1999;13:515-519.
77. Greenspan SL, Bone HG, Ettinger MP et al. Effect of recombinant human parathyroid hormone (1-84) on vertebral fracture and bone mineral density in postmenopausal women with osteoporosis: a randomized trial. Ann Intern Med 2007;146:326-339.
78. Smith JG, Merrill DC. Oxytocin for induction of labor. Clin Obstet Gynecol 2006;49:594-608.