N-Cadherin/Wnt Interaction Controls Bone Marrow Mesenchymal Cell Fate and Bone Mass During Aging

Journal of Cellular Physiology

Volumn 229, Issue 11, 2014, Pages 1765-1775

  Haÿ, Eric ^a,b   Dieudonné, François Xavier ^a,b   Saidak, Zuzana ^a,b   Marty, Caroline ^a,b   Brun, Julia ^a,b   Da Nascimento, Sophie ^c   Sonnet, Pascal ^c   Marie, Pierre J ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; CYCLIN D1; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; MYC PROTEIN; NERVE CELL ADHESION MOLECULE; OSTEOCALCIN; TRANSCRIPTION FACTOR RUNX2; WNT10B PROTEIN; WNT5A PROTEIN;

ADIPOCYTE; ADIPOGENESIS; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DENSITY; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; BONE MASS; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CONTROLLED STUDY; EMBRYO; FEMALE; MESENCHYME CELL; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPENIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; WNT SIGNALING PATHWAY;

ADIPOCYTES; ADIPOGENESIS; AGING; ANIMALS; BONE MARROW CELLS; BONE RESORPTION; CADHERINS; CELL DIFFERENTIATION; CELL LINEAGE; MESENCHYMAL STROMAL CELLS; MICE; MICE, TRANSGENIC; ORGAN SIZE; OSTEOBLASTS; OSTEOGENESIS; PROTEIN BINDING; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; WNT PROTEINS;

EID: 84904891746     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24629     Document Type: Article

References (50)

1. Arai F, Hosokawa K, Toyama H, Matsumoto Y, Suda T. 2012. Role of N-cadherin in the regulation of hematopoietic stem cells in the bone marrow niche. Ann NY Acad Sci 1266:72-77.
2. Askmyr M, Sims NA, Martin TJ, Purton LE. 2009. What is the true nature of the osteoblastic hematopoietic stem cell niche? Trends Endocrinol Metab 20:303-309.
3. Aubin JE. 2001. Regulation of osteoblast formation and function. Rev Endocr Metab Disord 2:81-94.
4. Baron R, Kneissel M. 2013. WNT signaling in bone homeostasis and disease: From human mutations to treatments. Nat Med 19:179-192.
5. Bennett CN, Longo KA, Wright WS, Suva LJ, Lane TF, Hankenson KD, MacDougald OA. 2005. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci USA 102:3324-3329.
6. Bennett CN, Ouyang H, Ma YL, Zeng Q, Gerin I, Sousa KM, Lane TF, Krishnan V, Hankenson KD, MacDougald OA. 2007. Wnt10b increases postnatal bone formation by enhancing osteoblast differentiation. J Bone Miner Res 22:1924-1932.
7. Bilkovski R, Schulte DM, Oberhauser F, Gomolka M, Udelhoven M, Hettich MM, Roth B, Heidenreich A, Gutschow C, Krone W, Laudes M. 2010. Role of WNT-5a in the determination of human mesenchymal stem cells into preadipocytes. J Biol Chem 285:6170-6178.
8. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT. 2003. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425:841-846.
9. Castro CH, Shin CS, Stains JP, Cheng SL, Sheikh S, Mbalaviele G, Szejnfeld VL, Civitelli R. 2004. Targeted expression of a dominant-negative N-cadherin in vivo delays peak bone mass and increases adipogenesis J Cell Sci 117:2853-2864.
10. Clement-Lacroix P, Ai M, Morvan F, Roman-Roman S, Vayssiere B, Belleville C, Estrera K, Warman ML, Baron R, Rawadi G. 2005. Lrp5-independent activation of Wnt signaling by lithium chloride increases bone formation and bone mass in mice. Proc Natl Acad Sci USA 102:17406-17411.
11. Duchartre Y, Petit N, Moya C, Lalanne M, Dubus P, Verneuil H, Moreau-Gaudry F, Richard E. 2011. Neonatal bone marrow transplantation prevents liver disease in a murine model of erythropoietic protoporphyria. J Hepatol 55:162-170.
12. French DM, Kaul RJ, D'Souza AL, Crowley CW, Bao M, Frantz GD, Filvaroff EH, Desnoyers L. 2004. WISP-1 is an osteoblastic regulator expressed during skeletal development and fracture repair. Am J Pathol 165:855-867.
13. Gimble JM, Robinson CE, Wu X, Kelly KA. 1996. The function of adipocytes in the bone marrow stroma: An update. Bone 19:421-428.
14. Gottardi CJ, Gumbiner BM. 2001. Adhesion signaling: How beta-catenin interacts with its partners. Curr Biol 11:R792-794.
15. Greenbaum AM, Revollo LD, Woloszynek JR, Civitelli R, Link DC. 2012. N-cadherin in osteolineage cells is not required for maintenance of hematopoietic stem cells. Blood 120:295-302.
16. Gunduz V, Kong E, Bryan CD, Hinds PW. 2012. Loss of the retinoblastoma tumor suppressor protein in murine calvaria facilitates immortalization of osteoblast- adipocyte bipotent progenitor cells characterized by low expression of N- cadherin. Mol Cell Biol 32:2561-2569.
17. Haug JS, He XC, Grindley JC, Wunderlich JP, Gaudenz K, Ross JT, Paulson A, Wagner KP, Xie Y, Zhu R, Yin T, Perry JM, Hembree MJ, Redenbaugh EP, Radice GL, Seidel C, Li L. 2008. N-cadherin expression level distinguishes reserved versus primed states of hematopoietic stem cells. Cell Stem Cell 2:367-379.
18. Haÿ E, Laplantine E, Geoffroy V, Frain M, Kohler T, Muller R, Marie PJ. 2009. N- cadherin interacts with axin and LRP5 to negatively regulate Wnt/beta-catenin signaling, osteoblast function, and bone formation. Mol Cell Biol 29:953-964.
19. Haÿ E, Nouraud A, Marie PJ. 2009. N-cadherin negatively regulates osteoblast proliferation and survival by antagonizing Wnt, ERK and PI3K/Akt signalling. PLoS One 4:e8284.
20. Haÿ E, Buczkowski T, Marty C, Da Nascimento S, Sonnet P, Marie PJ. 2012. Peptide-based mediated disruption of N-cadherin-LRP5/6 interaction promotes Wnt signaling and bone formation. J Bone Miner Res 27:1852-1863.
21. Jilka RL, Weinstein RS, Takahashi K, Parfitt AM, Manolagas SC. 1996. Linkage of decreased bone mass with impaired osteoblastogenesis in a murine model of accelerated senescence. J Clin Invest 97:1732-1740.
22. Justesen J, Stenderup K, Ebbesen EN, Mosekilde L, Steiniche T, Kassem M. 2001. Adipocyte tissue volume in bone marrow is increased with aging and in patients with osteoporosis. Biogerontology 2:165-171.
23. Kajkenova O, Lecka-Czernik B, Gubrij I, Hauser SP, Takahashi K, Parfitt AM, Jilka RL, Manolagas SC, Lipschitz DA. 1997. Increased adipogenesis and myelopoiesis in the bone marrow of SAMP6, a murine model of defective osteoblastogenesis and low turnover osteopenia. J Bone Miner Res 12:1772-1779.
24. Kang S, Bennett CN, Gerin I, Rapp LA, Hankenson KD, Macdougald OA. 2007. Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein alpha and peroxisome proliferator-activated receptor gamma. J Biol Chem 282:14515-14524.
25. Kawai M, Modder UI, Khosla S, Rosen CJ. 2011. Emerging therapeutic opportunities for skeletal restoration. Nat Rev Drug Discov 10:141-156.
26. Kiel MJ, Morrison SJ. 2008. Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 8:290-301.
27. Long F. 2011. Building strong bones: Molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol 13:27-38.
28. Marie PJ. 2002. Role of N-cadherin in bone formation. J Cell Physiol 190:297-305.
29. Marie PJ. 2008. Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys 473:98-105.
30. Martin TJ, Seeman E. 2008. Bone remodelling: its local regulation and the emergence of bone fragility. Best Pract Res Clin Endocrinol Metab 22:701-722.
31. Mbalaviele G, Shin CS, Civitelli R. 2006. Cell-cell adhesion and signaling through cadherins: connecting bone cells in their microenvironment. J Bone Miner Res 21:1821-1827.
32. Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma'ayan A, Enikolopov GN, Frenette PS. 2010. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466:829-834.
33. Moerman EJ, Teng K, Lipschitz DA, Lecka-Czernik B. 2004. Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: The role of PPAR-gamma2 transcription factor and TGF- beta/BMP signaling pathways. Aging Cell 3:379-389.
34. Nelson WJ, Nusse R. 2004. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303:1483-1487.
35. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. 1987. Bone histomorphometry: Standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595-610.
36. Qiu W, Andersen TE, Bollerslev J, Mandrup S, Abdallah BM, Kassem M. 2007. Patients with high bone mass phenotype exhibit enhanced osteoblast differentiation and inhibition of adipogenesis of human mesenchymal stem cells J Bone Miner Res 22:1720-1731.
37. Rosen CJ, Ackert-Bicknell C, Rodriguez JP, Pino AM. 2009. Marrow fat and the bone microenvironment: Developmental, functional, and pathological implications. Crit Rev Eukaryot Gene Expr 19:109-124.
38. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, Tagliafico E, Ferrari S, Robey PG, Riminucci M, Bianco P. 2007. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131:324-336.
39. Saidak Z, Hay E, Marty C, Barbara A, Marie PJ. 2012. Strontium ranelate rebalances bone marrow adipogenesis and osteoblastogenesis in senescent osteopenic mice through NFATc/Maf and Wnt signaling. Aging Cell 11:467-474.
40. Sims NA, Walsh NC. 2012. Intercellular cross-talk among bone cells: New factors and pathways. Curr Osteoporos Rep 10:109-117.
41. Song L, Liu M, Ono N, Bringhurst FR, Kronenberg HM, Guo J. 2012. Loss of wnt/beta-catenin signaling causes cell fate shift of preosteoblasts from osteoblasts to adipocytes. J Bone Miner Res 27:2344-2358.
42. Stevens JR, Miranda-Carboni GA, Singer MA, Brugger SM, Lyons KM, Lane TF. 2010. Wnt10b deficiency results in age-dependent loss of bone mass and progressive reduction of mesenchymal progenitor cells. J Bone Miner Res 25:2138-2147.
43. Takada I, Kouzmenko AP, Kato S. 2009. Wnt and PPARgamma signaling in osteoblastogenesis and adipogenesis. Nat Rev Rheumatol 5:442-447.
44. Takada I, Mihara M, Suzawa M, Ohtake F, Kobayashi S, Igarashi M, Youn MY, Takeyama K, Nakamura T, Mezaki Y, Takezawa S, Yogiashi Y, Kitagawa H, Yamada G, Takada S, Minami Y, Shibuya H, Matsumoto K, Kato S. 2007. A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat Cell Biol 9:1273-1285.
45. Tormin A, Li O, Brune JC, Walsh S, Schutz B, Ehinger M, Ditzel N, Kassem M, Scheding S. 2011. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood 117:5067-5077.
46. Wu JY, Scadden DT, Kronenberg HM. 2009. Role of the osteoblast lineage in the bone marrow hematopoietic niches. J Bone Miner Res 24:759-764.
47. Yin T, Li L. 2006. The stem cell niches in bone. J Clin Invest 116:1195-1201.
48. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, Li L. 2003. Identification of the haematopoietic stem cell niche and control of the niche size Nature 425:836-841.
49. Zhong Z, Zylstra-Diegel CR, Schumacher CA, Baker JJ, Carpenter AC, Rao S, Yao W, Guan M, Helms JA, Lane NE, Lang RA, Williams BO. 2012. Wntless functions in mature osteoblasts to regulate bone mass. Proc Natl Acad Sci USA 109:E2197-E2204.
50. Zylstra CR, Wan C, VanKoevering KK, Sanders AK, Lindvall C, Clemens TL, Williams BO. 2008. Gene targeting approaches in mice: assessing the roles of LRP5 and LRP6 in osteoblasts. J Musculoskelet Neuronal Interact 8:291-293.