DAP12 Overexpression Induces Osteopenia and Impaired Early Hematopoiesis

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Despars, Geneviève ^a,b   Pandruvada, Subramanya N M ^a,c   Anginot, Adrienne ^a,d   Domenget, Chantal ^a   Jurdic, Pierre ^a   Mazzorana, Marlène ^a  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL COUNT; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; CORTICAL BONE; FEMALE; HEMATOPOIESIS; HOMEOSTASIS; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOPENIA; OVARY FOLLICLE CELL; PHENOTYPE; PRE B LYMPHOCYTE; PROTEIN EXPRESSION; SPLEEN CELL; TRABECULAR BONE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BONE DISEASES, METABOLIC; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HEMATOPOIESIS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; OSTEOBLASTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLEEN;

ANIMALIA; MUS;

EID: 84878952511     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065297     Document Type: Article

References (44)

1. Lee SH, Rho J, Jeong D, Sul JY, Kim T, et al. (2006) v-ATPase V0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat Med 12: 1403-1409.
2. Zhao C, Irie N, Takada Y, Shimoda K, Miyamoto T, et al. (2006) Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 4: 111-121.
3. Feng X, McDonald JM, (2011) Disorders of bone remodeling. Annu Rev Pathol 6: 121-145.
4. Raisz LG, (2005) Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J Clin Invest 115: 3318-3325.
5. Boyle WJ, Simonet WS, Lacey DL, (2003) Osteoclast differentiation and activation. Nature 423: 337-342.
6. Akashi K, Traver D, Miyamoto T, Weissman IL, (2000) A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404: 193-197.
7. Hodge JM, Kirkland MA, Aitken CJ, Waugh CM, Myers DE, et al. (2004) Osteoclastic potential of human CFU-GM: biphasic effect of GM-CSF. J Bone Miner Res 19: 190-199.
8. Wang LD, Wagers AJ, (2004) Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat Rev Mol Cell Biol 12: 643-655.
9. Rivollier A, Mazzorana M, Tebib J, Piperno M, Aitsiselmi T, et al. (2004) Immature dendritic cell transdifferentiation into osteoclasts: a novel pathway sustained by the rheumatoid arthritis microenvironment. Blood 104: 4029-4037.
10. Speziani C, Rivollier A, Gallois A, Coury F, Mazzorana M, et al. (2007) Murine dendritic cell transdifferentiation into osteoclasts is differentially regulated by innate and adaptive cytokines. Eur J Immunol 37: 747-757.
11. Jurdic P, Saltel F, Chabadel A, Destaing O, (2006) Podosome and sealing zone: specificity of the osteoclast model. Eur J Cell Biol 85: 195-202.
12. Koga T, Inui M, Inoue K, Kim S, Suematsu A, et al. (2004) Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428: 758-763.
13. Shinohara M, Koga T, Okamoto K, Sakaguchi S, Arai K, et al. (2008) Tyrosine kinases Btk and Tec regulate osteoclast differentiation by linking RANK and ITAM signals. Cell 132: 794-806.
14. Humphrey MB, Lanier LL, Nakamura MC, (2005) Role of ITAM-containing adapter proteins and their receptors in the immune system and bone. Immunol Rev 208: 50-65.
15. Schleinitz N, Chiche L, Guia S, Bouvier G, Vernier J, et al. (2009) Pattern of DAP12 expression in leukocytes from both healthy and systemic lupus erythematosus patients. PLoS One 4: e6264.
16. Tomasello E, Vivier E, (2005) KARAP/DAP12/TYROBP: three names and a multiplicity of biological functions. Eur J Immunol 35: 1670-1677.
17. Paloneva J, Kestila M, Wu J, Salminen A, Bohling T, et al. (2000) Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat Genet 25: 357-361.
18. Paloneva J, Autti T, Raininko R, Partanen J, Salonen O, et al. (2001) CNS manifestations of Nasu-Hakola disease: a frontal dementia with bone cysts. Neurology 56: 1552-1558.
19. Humphrey MB, Ogasawara K, Yao W, Spusta SC, Daws MR, et al. (2004) The signaling adapter protein DAP12 regulates multinucleation during osteoclast development. J Bone Miner Res 19: 224-234.
20. Kaifu T, Nakahara J, Inui M, Mishima K, Momiyama T, et al. (2003) Osteopetrosis and thalamic hypomyelinosis with synaptic degeneration in DAP12-deficient mice. J Clin Invest 111: 323-332.
21. Mocsai A, Humphrey MB, Van Ziffle JA, Hu Y, Burghardt A, et al. (2004) The immunomodulatory adapter proteins DAP12 and Fc receptor gamma-chain (FcRgamma) regulate development of functional osteoclasts through the Syk tyrosine kinase. Proc Natl Acad Sci U S A 101: 6158-6163.
22. Nataf S, Anginot A, Vuaillat C, Malaval L, Fodil N, et al. (2005) Brain and bone damage in KARAP/DAP12 loss-of-function mice correlate with alterations in microglia and osteoclast lineages. Am J Pathol 166: 275-286.
23. Barrow AD, Raynal N, Andersen TL, Slatter DA, Bihan D,et al. OSCAR is a collagen receptor that costimulates osteoclastogenesis in DAP12-deficient humans and mice. J Clin Invest 121: 3505-3516.
24. Anginot A, Dacquin R, Mazzorana M, Jurdic P, (2007) Lymphocytes and the Dap12 adaptor are key regulators of osteoclast activation associated with gonadal failure. PLoS One 2: e585.
25. Wu Y, Torchia J, Yao W, Lane NE, Lanier LL, et al. (2007) Bone microenvironment specific roles of ITAM adapter signaling during bone remodeling induced by acute estrogen-deficiency. PLoS One 2: e586.
26. Lucas M, Daniel L, Tomasello E, Guia S, Horschowski N, et al. (2002) Massive inflammatory syndrome and lymphocytic immunodeficiency in KARAP/DAP12-transgenic mice. Eur J Immunol 32: 2653-2663.
27. David V, Laroche N, Boudignon B, Lafage-Proust MH, Alexandre C, et al. (2003) Noninvasive in vivo monitoring of bone architecture alterations in hindlimb-unloaded female rats using novel three-dimensional microcomputed tomography. J Bone Miner Res 18: 1622-1631.
28. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, et al. (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2: 595-610.
29. Kulterer B, Friedl G, Jandrositz A, Sanchez-Cabo F, Prokesch A, et al. (2007) Gene expression profiling of human mesenchymal stem cells derived from bone marrow during expansion and osteoblast differentiation. BMC Genomics 8: 70.
30. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, et al. (2006) Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 12: 657-664.
31. Cho KA, Joo SY, Han HS, Ryu KH, Woo SY, (2010) Osteoclast activation by receptor activator of NF-kappaB ligand enhances the mobilization of hematopoietic progenitor cells from the bone marrow in acute injury. Int J Mol Med 26: 557-563.
32. Kotani M, Kikuta J, Klauschen F, Chino T, Kobayashi Y, et al. (2013) Systemic circulation and bone recruitment of osteoclast precursors tracked by using fluorescent imaging techniques. J Immunol 190: 605-612.
33. Li Y, Toraldo G, Li A, Yang X, Zhang H, et al. (2007) B cells and T cells are critical for the preservation of bone homeostasis and attainment of peak bone mass in vivo. Blood 109: 3839-3848.
34. Kiani A, Habermann I, Haase M, Feldmann S, Boxberger S, et al. (2004) Expression and regulation of NFAT (nuclear factors of activated T cells) in human CD34+ cells: down-regulation upon myeloid differentiation. J Leukoc Biol 76: 1057-1065.
35. Kiani A, Kuithan H, Kuithan F, Kyttala S, Habermann I, et al. (2007) Expression analysis of nuclear factor of activated T cells (NFAT) during myeloid differentiation of CD34+ cells: regulation of Fas ligand gene expression in megakaryocytes. Exp Hematol 35: 757-770.
36. Muller MR, Sasaki Y, Stevanovic I, Lamperti ED, Ghosh S, et al. (2009) Requirement for balanced Ca/NFAT signaling in hematopoietic and embryonic development. Proc Natl Acad Sci U S A 106: 7034-7039.
37. Bauer W, Rauner M, Haase M, Kujawski S, Arabanian LS, et al. (2011) Osteomyelosclerosis, anemia and extramedullary hematopoiesis in mice lacking the transcription factor NFATc2. Haematologica 96: 1580-1588.
38. Nagasawa T, (2006) Microenvironmental niches in the bone marrow required for B-cell development. Nat Rev Immunol 6: 107-116.
39. Mourcin F, Breton C, Tellier J, Narang P, Chasson L, et al. (2011) Galectin-1-expressing stromal cells constitute a specific niche for pre-BII cell development in mouse bone marrow. Blood 117: 6552-6561.
40. Takeshita S, Namba N, Zhao JJ, Jiang Y, Genant HK, et al. (2002) SHIP-deficient mice are severely osteoporotic due to increased numbers of hyper-resorptive osteoclasts. Nat Med 8: 943-949.
41. Helgason CD, Kalberer CP, Damen JE, Chappel SM, Pineault N, et al. (2000) A dual role for Src homology 2 domain-containing inositol-5-phosphatase (SHIP) in immunity: aberrant development and enhanced function of b lymphocytes in ship -/- mice. J Exp Med 191: 781-794.
42. Nakamura K, Kouro T, Kincade PW, Malykhin A, Maeda K, et al. (2004) Src homology 2-containing 5-inositol phosphatase (SHIP) suppresses an early stage of lymphoid cell development through elevated interleukin-6 production by myeloid cells in bone marrow. J Exp Med 199: 243-254.
43. Helgason CD, Damen JE, Rosten P, Grewal R, Sorensen P, et al. (1998) Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev 12: 1610-1620.
44. Peng Q, Malhotra S, Torchia JA, Kerr WG, Coggeshall KM, et al. (2010) TREM2- and DAP12-dependent activation of PI3K requires DAP10 and is inhibited by SHIP1. Sci Signal 3: ra38.