Caspase-1 Mediated Cleavage of BMP Type I Receptor Drives BMP2-Induced Differentiation of Bone Marrow Mesenchymal Stem Cells into Adipocytes
Source abstract
Abstract
Bone Morphogenetic Protein-2 (BMP2) is a growth factor that maintains bone homeostasis through the BMP receptor type Ia (BMPRIa) and type II (BMPRII). BMP2 promotes osteogenesis by inducing the differentiation of bone marrow mesenchymal stem cells (BMSCs) into osteoblasts; however, it can also trigger BMSC differentiation into adipocytes. BMP2’s osteo-inductive ability has made it a potential treatment for osteoporosis, yet its dual role in BMSC differentiation complicates its efficacy. High BMP2 levels cause BMPRIa cleavage, but the downstream effects and the mechanisms governing BMP2-induced osteogenesis or adipogenesis are unresolved. Here, we identify Caspase-1 as a key mediator of BMPRIa cleavage and its downstream effects on adipogenesis. We used primary BMSCs from C57BL/6 mice, stimulated with varying BMP2 concentrations, to explore BMP2-induced BMPRIa cleavage and its impact on PPARγ—a key regulator of adipogenesis. Western blotting and immunostaining using antibodies against BMPRIa and PPARγ uncovered BMPRIa cleavage and revealed the nuclear translocation of the cleaved segment, colocalizing with PPARγ. Caspase-1 inhibition significantly reduced BMPRIa cleavage and PPARγ expression, highlighting its pivotal role in adipogenic differentiation. Understanding the molecular mechanisms of BMP2-induced adipogenesis and Caspase-1 inhibition could improve BMP2 therapeutic efficacy for osteoporosis by promoting osteogenesis over adipogenesis.
Source: crossref · Quality: baseline
Research context
OpenAlex topics: TGF-β signaling in diseases · Bone Metabolism and Diseases · Bone health and osteoporosis research
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
Department of Biological Sciences, University of Delaware, Newark, DE 19716, USA
Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA
Funding
National Institute of Arthritis and Musculoskeletal and Skin Diseases · the Nathan Shock Center Pilot Award; and the Institutional Development Award (IDeA) from the National Institute of Health’s General Medical Sciences
References (60)
Show source-provided references
1. Fu, X., Liu, G., Halim, A., Ju, Y., Luo, Q., Song, G., Fu, X., Liu, G., Halim, A., and Ju, Y. (2019). Mesenchymal Stem Cell Migration and Tissue Repair. Cells, 8.10.3390/cells8080784 ↗
2. Biological functions of mesenchymal stem cells and clinical implications10.1007/s00018-019-03125-1 ↗
3. Arthur, A., Gronthos, S., Arthur, A., and Gronthos, S. (2020). Clinical Application of Bone Marrow Mesenchymal Stem/Stromal Cells to Repair Skeletal Tissue. Int. J. Mol. Sci., 21.10.3390/ijms21249759 ↗
4. Immunoregulatory mechanisms of mesenchymal stem and stromal cells in inflammatory diseases10.1038/s41581-018-0023-5 ↗
5. Enhanced Osteogenic Differentiation of Human Bone Marrow Mesenchymal Stem Cells in Ossification of the Posterior Longitudinal Ligament Through Activation of the BMP2-Smad1/5/8 Pathway10.1089/scd.2020.0117 ↗
6. Komori, T., and Komori, T. (2019). Regulation of Proliferation, Differentiation and Functions of Osteoblasts by Runx2. Int. J. Mol. Sci., 20.10.3390/ijms20071694 ↗
7. PPAR-γ and Wnt Regulate the Differentiation of MSCs into Adipocytes and Osteoblasts Respectively10.2174/1574888X12666171012141908 ↗
8. Molecular Mechanisms of PPAR-γ Governing MSC Osteogenic and Adipogenic Differentiation10.2174/1574888X10666150531173309 ↗
9. Expression of RUNX2 and Osterix in Rat Mesenchymal Stem Cells During Culturing in Osteogenic-Conditioned Medium10.1007/s10517-020-04931-5 ↗
10. Role of Marrow Adipocytes in Regulation of Energy Metabolism and Bone Homeostasis10.1007/s11914-018-0425-0 ↗
11. Osteoporosis-associated alteration in the signalling status of BMP-2 in human MSCs under adipogenic conditions10.1002/jcb.25082 ↗
12. The relationship between bone marrow adipose tissue and bone metabolism in postmenopausal osteoporosis10.1016/j.cytogfr.2020.02.003 ↗
13. Durbano, H.W., Halloran, D., Nguyen, J., Stone, V., Mctague, S., Eskander, M., and Nohe, A. (2020). Aberrant BMP2 Signaling in Patients Diagnosed with Osteoporosis. Int. J. Mol. Sci., 21.10.3390/ijms21186909 ↗
14. The Recent Prevalence of Osteoporosis and Low Bone Mass in the United States Based on Bone Mineral Density at the Femoral Neck or Lumbar Spine10.1002/jbmr.2269 ↗
15. Primary osteoporosis in postmenopausal women
16. Rheumatoid arthritis and osteoporosis10.1007/s003930070036 ↗
17. Li, J., Hu, Y., You, H., Li, R., Ran, Q., Ouyang, T., and Huang, Y. (2023). Trabecular Bone Microarchitecture Evaluation in an Osteoporosis Mouse Model. J. Vis. Exp., e65880.10.3791/65880 ↗
18. American Association of Clinical Endocrinologists/American College of Endocrinology Clinical Practice Guidelines for the Diagnosis and Treatment of Postmenopausal Osteoporosis—2020 Update10.4158/GL-2020-0524SUPPL ↗
19. Halloran, D., Pandit, V., Macmurray, C., Stone, V., Degeorge, K., Eskander, M., Root, D., Mctague, S., Pelkey, H., and Nohe, A. (2022). Age-Related Low Bone Mineral Density in C57BL/6 Mice Is Reflective of Aberrant Bone Morphogenetic Protein-2 Signaling Observed in Human Patients Diagnosed with Osteoporosis. Int. J. Mol. Sci., 23.10.3390/ijms231911205 ↗
20. The Clinical Effectiveness of Denosumab (Prolia®) for the Treatment of Osteoporosis in Postmenopausal Women, Compared to Bisphosphonates, Selective Estrogen Receptor Modulators (SERM), and Placebo: A Systematic Review and Network Meta-Analysis10.1007/s00223-023-01078-z ↗
21. Bone Health and Osteoporosis Prevention and Treatment10.1097/GRF.0000000000000572 ↗
22. Economic burden of osteoporosis in the world: A systematic review
23. Bone Morphogenetic Protein (BMP) signaling in development and human diseases10.1016/j.gendis.2014.07.005 ↗
24. BMP signaling in development and diseases: A pharmacological perspective10.1016/j.bcp.2013.01.004 ↗
25. The TGFbeta Superfamily Signaling Pathway10.1002/wdev.86 ↗
26. TGF-β and BMP Signaling in Osteoblast Differentiation and Bone Formation10.7150/ijbs.2929 ↗
27. Transforming Growth Factor Beta Family: Insight into the Role of Growth Factors in Regulation of Fracture Healing Biology and Potential Clinical Applications10.1155/2015/137823 ↗
28. Halloran, D., Durbano, H.W., and Nohe, A. (2020). Bone Morphogenetic Protein-2 in Development and Bone Homeostasis. J. Dev. Biol., 8.10.3390/jdb8030019 ↗
29. Beiranvand, S., Hasanzadeh-Kiabi, F., Beiranvand, S., and Hasanzadeh-Kiabi, F. (2021). Application of Bone Morphogenetic Protein in Spinal Fusion Surgery; Minimally Invasive Spine Surgery—Advances and Innovations, IntechOpen.10.5772/intechopen.96883 ↗
30. BMPRIA is required for osteogenic differentiation and RANKL expression in adult bone marrow mesenchymal stromal cells10.1038/s41598-018-26820-8 ↗
31. Gu, S., Wu, W., Liu, C., Yang, L., Sun, C., Ye, W., Li, X., Chen, J., Long, F., and Chen, Y. (2014). BMPRIA Mediated Signaling Is Essential for Temporomandibular Joint Development in Mice. PLoS ONE, 9.10.1371/journal.pone.0101000 ↗
32. Turning Bone Morphogenetic Protein 2 (BMP2) On and Off in Mesenchymal Cells10.1002/jcb.25164 ↗
33. Structural basis for ALK2/BMPR2 receptor complex signaling through kinase domain oligomerization10.1038/s41467-021-25248-5 ↗
34. Type II BMP and activin receptors BMPR2 and ACVR2A share a conserved mode of growth factor recognition10.1016/j.jbc.2022.102076 ↗
35. Smad-independent TGF-β2 signaling pathways in human trabecular meshwork cells10.1016/j.exer.2016.07.012 ↗
36. Trapping of BMP receptors in distinct membrane domains inhibits their function in pulmonary arterial hypertension10.1152/ajplung.00300.2010 ↗
37. Bone Morphogenetic Protein Receptor Type Ia Localization Causes Increased BMP2 Signaling in Mice Exhibiting Increased Peak Bone Mass Phenotype10.1002/jcp.23028 ↗
38. Initiation of BMP2 Signaling in Domains on the Plasma Membrane10.1002/jcp.23032 ↗
39. Caveolae regulate smad signaling as verified by novel imaging and system biology approaches10.1002/jcp.24253 ↗
40. Conditioned medium from bone marrow-derived mesenchymal stem cells inhibits vascular calcification through blockade of the BMP2–Smad1/5/8 signaling pathway10.1186/s13287-018-0894-1 ↗
41. Casein kinase 2 regulates in vivo bone formation through its interaction with bone morphogenetic protein receptor type Ia10.1016/j.bone.2011.06.037 ↗
42. Casein Kinase 2 β-Subunit Is a Regulator of Bone Morphogenetic Protein 2 Signaling10.1016/j.bpj.2010.04.070 ↗
43. Bone Morphogenetic Proteins: A critical review10.1016/j.cellsig.2010.10.003 ↗
44. RhBMP-2-induced radiculitis in patients undergoing transforaminal lumbar interbody fusion: Relationship to dose10.1016/j.spinee.2016.06.007 ↗
45. Bone morphogenetic protein (BMP)9 in cancer development: Mechanistic, diagnostic, and therapeutic approaches?10.1080/1061186X.2023.2236330 ↗
46. A Review of the Clinical Side Effects of Bone Morphogenetic Protein-210.1089/ten.teb.2015.0357 ↗
47. Inhibition of CK2 binding to BMPRIa induces C2C12 differentiation into osteoblasts and adipocytes10.1007/s12079-013-0199-1 ↗
48. The Inflammasome-Mediated Caspase-1 Activation Controls Adipocyte Differentiation and Insulin Sensitivity10.1016/j.cmet.2010.11.011 ↗
49. Caspase-1 as a regulatory molecule of lipid metabolism10.1186/s12944-020-01220-y ↗
50. Wang, Y., Chen, G., Xu, M., Cui, Y., He, W., Zeng, H., Zeng, T., Cheng, R., Li, X., and Wang, Y. (2024). Caspase-1 Deficiency Modulates Adipogenesis Through Atg7-Mediated Autophagy: An Inflammatory-Independent Mechanism. Biomolecules, 14.10.3390/biom14040501 ↗
51. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S.e., Wilkins, M.R., Appel, R.D., and Bairoch, A. (2005). Protein Identification and Analysis Tools on the ExPASy Server. The Proteomics Protocols Handbook, Humana Press.10.1385/1-59259-890-0:571 ↗
52. Prolyl Oligopeptidase10.1016/S0092-8674(00)81416-6 ↗
53. Aging and bone10.1177/0022034510377791 ↗
54. Age-related behavioral changes from young to old age in male mice of a C57BL/6J strain maintained under a genetic stability program10.1002/npr2.12052 ↗
55. Adipocyte Accumulation in the Bone Marrow during Obesity and Aging Impairs Stem Cell-Based Hematopoietic and Bone Regeneration10.1016/j.stem.2017.02.009 ↗
56. Fate decision of mesenchymal stem cells: Adipocytes or osteoblasts?10.1038/cdd.2015.168 ↗
57. Signaling Crosstalk Between PPARγ and BMP2 in Mesenchymal Stem Cells10.1155/2012/607141 ↗
58. A new MMP-mediated prodomain cleavage mechanism to activate bone morphogenetic proteins from the extracellular matrix10.1096/fj.202001264R ↗
59. Caspase-1 as a multifunctional inflammatory mediator: Noncytokine maturation roles10.1189/jlb.3MR0516-224R ↗
60. The Canonical Notch Signaling Pathway: Unfolding the Activation Mechanism10.1016/j.cell.2009.03.045 ↗