Biology:Bone marrow adipose tissue

From HandWiki
Bone marrow adipose tissue
Details
SystemMusculoskeletal (or Locomotor)
Identifiers
LatinAdipose Ossium Medulla
Anatomical terminology
Bone marrow adipocytes are derived from mesenchymal stem cell (MSC) differentiation.

Bone marrow adipose tissue (BMAT), sometimes referred to as marrow adipose tissue (MAT), is a type of fat deposit in bone marrow. It increases in states of low bone density -osteoporosis,[1][2] anorexia nervosa/ caloric restriction,[3][4] skeletal unweighting such as that which occurs in space travel,[5][6] and anti-diabetes therapies.[7] BMAT decreases in anaemia, leukaemia, and hypertensive heart failure; in response to hormones such as oestrogen, leptin, and growth hormone; with exercise-induced weight loss or bariatric surgery; in response to chronic cold exposure; and in response to pharmacological agents such as bisphosphonates, teriparatide, and metformin.[8]

Anatomy

Bone marrow adipocytes (BMAds)[9] originate from mesenchymal stem cell (MSC) progenitors that also give rise to osteoblasts, among other cell types.[10] Thus, it is thought that BMAT results from preferential MSC differentiation into the adipocyte, rather than osteoblast, lineage in the setting of osteoporosis.[11] Since BMAT is increased in the setting of obesity[12][13][14] and is suppressed by endurance exercise,[15][12][16][17] or vibration,[18] it is likely that BMAT physiology, in the setting of mechanical input/exercise, approximates that of white adipose tissue (WAT).

Physiology

Exercise regulation

The first study to demonstrate exercise regulation of BMAT in rodents was published in 2014;[12] Now, exercise regulation of BMAT has been confirmed in a human,[19] adding clinical importance. Several studies demonstrated exercise reduction of BMAT which occurs along with an increase in bone quantity.[17][15][16][20] Since exercise increases bone quantity, reduces BMAT and increases expression of markers of fatty acid oxidation in bone, BMAT is thought to be providing needed fuel for exercise-induced bone formation or anabolism.[16] A notable exception occurs in the setting of caloric restriction: exercise suppression of BMAT does not yield an increase in bone formation and even appears to cause bone loss.[4][21][20] Indeed, energy availability appears to be a factor in the ability of exercise to regulate BMAT.[4] Another exception occurs in Lipodystrophy, a condition with reduced overall adipose stores: exercise- induced anabolism is possible, even with minimal BMAT stores.[22]

Relationships to other types of fat

BMAT has been reported to have qualities of both white and brown fat.[23] However, more-recent functional and -omics studies have shown that BMAT is a unique adipose depot that is molecularly and functionally distinct to WAT or BAT.[24][25][26][27] Subcutaneous white fat contain excess energy, indicating a clear evolutionary advantage during times of scarcity. WAT is also the source of adipokines and inflammatory markers which have both positive (e.g., adiponectin)[28] and negative[29] effects on metabolic and cardiovascular endpoints. Visceral abdominal fat (VAT) is a distinct type of WAT that is "proportionally associated with negative metabolic and cardiovascular morbidity",[30] regenerates cortisol,[31] and recently has been tied to decreased bone formation[32][33] Both types of WAT substantially differ from brown adipose tissue (BAT) as by a group of proteins that help BAT's thermogenic role.[34] BMAT, by its "specific marrow location, and its adipocyte origin from at least LepR+ marrow MSC is separated from non-bone fat storage by larger expression of bone transcription factors",[35] and likely indicates a different fat phenotype.[36] Recently, BMAT was noted to "produce a greater proportion of adiponectin – an adipokine associated with improved metabolism – than WAT",[37] suggesting an endocrine function for this depot, akin, but different, from that of WAT.

Impact on bone health

BMAT increases in states of bone fragility. BMAT is thought to result from preferential MSC differentiation into an adipocyte, rather than osteoblast lineage in osteoporosis[11][20] based on the inverse relationship between bone and BMAT in bone-fragile osteoporotic states. An increase in BMAT is noted in osteoporosis clinical studies measured by MR Spectroscopy.[38][39][40] Estrogen therapy in postmenopausal osteoporosis reduces BMAT.[41] Antiresorptive therapies like risedronate or zoledronate also decrease BMAT while increasing bone density, supporting an inverse relationship between bone quantity and BMAT. During aging, bone quantity declines[42][43] and fat redistributes from subcutaneous to ectopic sites such as bone marrow, muscle, and liver.[44] Aging is associated with lower osteogenic and greater adipogenic biasing of MSC.[45] This aging-related biasing of MSC away from osteoblast lineage may represent higher basal PPARγ expression[46] or decreased Wnt10b.[47][48][49] Thus, bone fragility, osteoporosis, and osteoporotic fractures are thought to be linked to mechanisms which promote BMAT accumulation.[citation needed]

Maintenance of hematopoietic stem cells

BMAds secrete factors that promote HSC renewal in most bones.[50]

Hematopoietic cells (also known as blood cells) reside in the bone marrow along with BMAds. These hematopoietic cells are derived from hematopoietic stem cells (HSC) which give rise to diverse cells: cells of the blood, immune system, as well as cells that break down bone (osteoclasts). HSC renewal occurs in the marrow stem cell niche, a microenvironment that contains cells and secreted factors that promote appropriate renewal and differentiation of HSC. The study of the stem cell niche is relevant to the field of oncology in order to improve therapy for multiple hematologic cancers. As such cancers are often treated with bone marrow transplantation, there is interest in improving the renewal of HSC.[citation needed]

Measurement

In order to understand the physiology of BMAT, various analytic methods have been applied. BMAds are difficult to isolate and quantify because they are interspersed with bony and hematopoietic elements. Until recently, qualitative measurements of BMAT have relied on bone histology,[51][52] which is subject to site selection bias and cannot adequately quantify the volume of fat in the marrow. Nevertheless, histological techniques and fixation make possible visualization of BMAT, quantification of BMAd size, and BMAT's association with the surrounding endosteum, milieu of cells, and secreted factors.[53][54][55]

Recent advances in cell surface and intracellular marker identification and single-cell analyses led to greater resolution and high-throughput ex-vivo quantification. Flow cytometric quantification can be used to purify adipocytes from the stromal vascular fraction of most fat depots.[56] Early research with such machinery cited adipocytes as too large and fragile for cytometer-based purification, rendering them susceptible to lysis; however, recent advances have been made to mitigate this;[57] nevertheless, this methodology continues to pose technical challenges[58] and is inaccessible to much of the research community.

To improve quantification of BMAT, novel imaging techniques have been developed as a means to visualize and quantify BMAT. Although proton magnetic resonance spectroscopy (1H-MRS) has been used with success to quantify vertebral BMAT in humans,[59] it is difficult to employ in laboratory animals.[60] Magnetic resonance imaging (MRI) provides BMAT assessment in the vertebral skeleton[61] in conjunction with μCT-based marrow density measurements.[62] A volumetric method to identify, quantify, and localize BMAT in rodent bone has been recently developed, requiring osmium staining of bones and μCT imaging,[63] followed by advanced image analysis of osmium-bound lipid volume (in mm3) relative to bone volume.[12][16][15] This technique provides reproducible quantification and visualization of BMAT, enabling the ability to consistently quantify changes in BMAT with diet, exercise, and agents that constrain precursor lineage allocation. Although the osmium method is quantitatively precise, osmium is toxic and cannot be compared across batched experiments. Recently, researchers developed and validated[16] a 9.4T MRI scanner technique that allows localization and volumetric (3D) quantification that can be compared across experiments, as in.[4]

Several studies have also analysed BMAT function in vivo using positron emission tomography - computed tomography (PET-CT) combined with the tracer 18F-Fluorodeoxyglucose (FDG). This allows glucose uptake, a measure of metabolic activity, to be quantified in living organisms, including humans. Two recent studies found that, unlike brown adipose tissue, BMAT does not increase glucose uptake in response to cold exposure, demonstrating that BMAT is functionally distinct from BAT.[24][64] The full extent of BMAT's impact on systemic metabolic homeostasis remains to be determined.

  • Methods for Quantification of Bone Marrow Adipose Tissue (BMAT)
  • Demonstration of Osmium-μCT method with Advanced Image Processing

    This figure demonstrates the use of the osmium- μCT method with advanced image processing to quantify BMAT. In this figure, running exercise is shown to suppress BMAT despite PPARγ agonist. Fat binder osmium is imaged via μCT (A ) in n =5 per group overlaid images. Quantification of osmium as BMAT/ bone volume in the whole femur is shown. a, significant due to Rosi. b, significant due to exercise. Rosi=rosiglizaone, CTL=control, E=exercise.

  • This figure demonstrates the use of MRI imaging (9.4T scanner) along with advanced image processing to quantify BMAT. The images and graph demonstrate that BMAT is higher in obese compared with lean mice. B6 mice were fed HFD from age 4 wk until age 16 wk. BMAT was quantified by MRI. A) n=10 superimposed group average images are shown B) BMAT normalized to bone volume in each group.

  • Representative distal femur histologic section of a 16-week-old healthy C57BL/6 mouse demonstrating a typical quantity of marrow adipocytes.

  • Representative distal femur histologic section of a 16-week-old C57BL/6 mouse after 6 weeks of calorie restriction demonstrating an increased quantity of marrow adipocytes.

Scientific Societies

The International Bone Marrow Adiposity Society (BMAS)

Because of the increasing interest in BMAT from both researchers and clinicians, in 2018 The International Bone Marrow Adiposity Society (BMAS) was founded.[65] Work to build the society began in Lille, France in 2015, when the first International Meeting on Bone Marrow Adiposity (BMA2015) was held. The meeting was a great success and led to a second international meeting (BMA2016) in August 2016 held in Rotterdam, The Netherlands. Both meetings were a success in that they for the first time brought together scientists and physicians from different backgrounds (bone metabolism, cancer, obesity and diabetes) to share ideas and advance research into, and our understanding of, the patho/physiological role of BMAds.

Logo for The International Bone Marrow Adiposity Society
Logo for The International Bone Marrow Adiposity Society

This success led to a network of researchers discussing the formation of a new society, focusing on bone marrow adiposity (BMA). This network worked together in 2016–2017 to lay the foundations for this society, which was then discussed further during the third international meeting held in Lausanne, Switzerland in 2017 (BMA2017). The statues were then signed at the fourth international meeting, held in 2018 again in Lille (BMA2018). As discussed in the following section, there have since been three further international meetings, held in Odense, Denmark in 2019 (BMA2019), virtually in 2020 (BMA2020), and in Athens, Greece in 2022 (BMA2022). The first BMAS Summer School was held virtually in the summer of 2021.

Since its foundation, BMAS working groups have published three position papers relating to nomenclature,[9] methodologies [66] and biobanking for BMA research.[67] These working groups remain active, with other working groups also focussing on clinical and translational issues, public engagement, and young researchers (Next Generation BMAS)

BMAS meetings

  • BMA2015 (Lille, France)[68]
  • BMA2016 (Rotterdam, Netherlands)[69]
  • BMA2017 (Lausanne, Switzerland)[70]
  • BMA2018 (Lille, France)[71]
  • BMA2019 (Odense, Denmark)
  • BMA2020 (virtual BMA meeting)[72]
  • BMA Summer School 2021 (virtual)[73]
  • BMA2022 (Athens, Greece)

American Society for Bone and Mineral Research

ASBMR has published hundreds of presentations and articles on BMAT featured in the ASBMR annual meetings, The Journal of Bone and Mineral Research ( JBMR) , JBMRPlus, and the Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism.

Endocrine Society

Endocrine society features many presentations and articles on BMAT.

References

  1. ↑ "Increased marrow adiposity in premenopausal women with idiopathic osteoporosis". The Journal of Clinical Endocrinology and Metabolism 97 (8): 2782–2791. August 2012. doi:10.1210/jc.2012-1477. PMID 22701013. 
  2. ↑ "Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies". Clinical Orthopaedics and Related Research 80: 147–154. October 1971. doi:10.1097/00003086-197110000-00021. PMID 5133320. 
  3. ↑ "Marrow fat and bone--new perspectives". The Journal of Clinical Endocrinology and Metabolism 98 (3): 935–945. March 2013. doi:10.1210/jc.2012-3634. PMID 23393168. 
  4. ↑ 4.0 4.1 4.2 4.3 "Exercise Degrades Bone in Caloric Restriction, Despite Suppression of Marrow Adipose Tissue (MAT)". Journal of Bone and Mineral Research 35 (1): 106–115. January 2020. doi:10.1002/jbmr.3872. PMID 31509274. 
  5. ↑ "Transforming growth factor beta2 inhibits adipocyte differentiation induced by skeletal unloading in rat bone marrow stroma". Journal of Bone and Mineral Research 17 (4): 668–677. April 2002. doi:10.1359/jbmr.2002.17.4.668. PMID 11918224. 
  6. ↑ "Skeletal abnormalities in rats induced by simulated weightlessness". Metabolic Bone Disease & Related Research 4 (1): 69–75. 1982-01-01. doi:10.1016/0221-8747(82)90011-X. PMID 7121257. 
  7. ↑ "Effects of rosiglitazone vs metformin on circulating osteoclast and osteogenic precursor cells in postmenopausal women with type 2 diabetes mellitus". The Journal of Clinical Endocrinology and Metabolism 99 (10): E1933–E1942. October 2014. doi:10.1210/jc.2013-3666. PMID 24905061. 
  8. ↑ "Bone Marrow Adipose Tissue". Encyclopedia of Bone Biology. Oxford, UK: Academic Press. 2020. pp. 156–177. doi:10.1016/B978-0-12-801238-3.11207-3. ISBN 978-0-12-814082-6. https://doi.org/10.1016/B978-0-12-801238-3.11207-3. 
  9. ↑ 9.0 9.1 "Standardised Nomenclature, Abbreviations, and Units for the Study of Bone Marrow Adiposity: Report of the Nomenclature Working Group of the International Bone Marrow Adiposity Society". Frontiers in Endocrinology 10: 923. 2020. doi:10.3389/fendo.2019.00923. PMID 32038486. 
  10. ↑ "Adipocyte differentiation of bone marrow-derived mesenchymal stem cells: cross talk with the osteoblastogenic program". Cellular and Molecular Life Sciences 66 (2): 236–253. January 2009. doi:10.1007/s00018-008-8429-z. PMID 18854943. 
  11. ↑ 11.0 11.1 "The Role of Bone Marrow Fat in Skeletal Health: Usefulness and Perspectives for Clinicians". The Journal of Clinical Endocrinology and Metabolism 100 (10): 3613–3621. October 2015. doi:10.1210/jc.2015-2338. PMID 26244490. 
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  14. ↑ "A High Fat Diet Increases Bone Marrow Adipose Tissue (MAT) But Does Not Alter Trabecular or Cortical Bone Mass in C57BL/6J Mice". Journal of Cellular Physiology 230 (9): 2032–2037. September 2015. doi:10.1002/jcp.24954. PMID 25663195. 
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  16. ↑ 16.0 16.1 16.2 16.3 16.4 "Exercise Decreases Marrow Adipose Tissue Through ß-Oxidation in Obese Running Mice". Journal of Bone and Mineral Research 32 (8): 1692–1702. August 2017. doi:10.1002/jbmr.3159. PMID 28436105. 
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  20. ↑ 20.0 20.1 20.2 "Exercise and Diet: Uncovering Prospective Mediators of Skeletal Fragility in Bone and Marrow Adipose Tissue". Current Osteoporosis Reports 18 (6): 774–789. December 2020. doi:10.1007/s11914-020-00634-y. PMID 33068251. 
  21. ↑ "Energy Deficiency Suppresses Bone Turnover in Exercising Women With Menstrual Disturbances". The Journal of Clinical Endocrinology and Metabolism 104 (8): 3131–3145. August 2019. doi:10.1210/jc.2019-00089. PMID 30896746. 
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  29. ↑ "Adipocytokines: mediators linking adipose tissue, inflammation and immunity". Nature Reviews. Immunology 6 (10): 772–783. October 2006. doi:10.1038/nri1937. PMID 16998510. 
  30. ↑ "Structural and biochemical characteristics of various white adipose tissue depots". Acta Physiologica 205 (2): 194–208. June 2012. doi:10.1111/j.1748-1716.2012.02409.x. PMID 22226221. 
  31. ↑ "A transgenic model of visceral obesity and the metabolic syndrome". Science 294 (5549): 2166–2170. December 2001. doi:10.1126/science.1066285. PMID 11739957. Bibcode: 2001Sci...294.2166M. 
  32. ↑ "Determinants of bone microarchitecture and mechanical properties in obese men". The Journal of Clinical Endocrinology and Metabolism 97 (11): 4115–4122. November 2012. doi:10.1210/jc.2012-2246. PMID 22933540. 
  33. ↑ "Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study". The Journal of Clinical Endocrinology and Metabolism 98 (6): 2562–2572. June 2013. doi:10.1210/jc.2013-1047. PMID 23515452. 
  34. ↑ "Adaptive thermogenesis in adipocytes: is beige the new brown?". Genes & Development 27 (3): 234–250. February 2013. doi:10.1101/gad.211649.112. PMID 23388824. 
  35. ↑ "Human stromal (mesenchymal) stem cells from bone marrow, adipose tissue and skin exhibit differences in molecular phenotype and differentiation potential". Stem Cell Reviews and Reports 9 (1): 32–43. February 2013. doi:10.1007/s12015-012-9365-8. PMID 22529014. 
  36. ↑ "Playing with bone and fat". Journal of Cellular Biochemistry 98 (2): 251–266. May 2006. doi:10.1002/jcb.20777. PMID 16479589. 
  37. ↑ "Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction". Cell Metabolism 20 (2): 368–375. August 2014. doi:10.1016/j.cmet.2014.06.003. PMID 24998914. 
  38. ↑ "Effects of risedronate on bone marrow adipocytes in postmenopausal women". Osteoporosis International 22 (5): 1547–1553. May 2011. doi:10.1007/s00198-010-1353-8. PMID 20661545. 
  39. ↑ "Osteoporosis is associated with increased marrow fat content and decreased marrow fat unsaturation: a proton MR spectroscopy study". Journal of Magnetic Resonance Imaging 22 (2): 279–285. August 2005. doi:10.1002/jmri.20367. PMID 16028245. 
  40. ↑ "Quantification of vertebral bone marrow fat content using 3 Tesla MR spectroscopy: reproducibility, vertebral variation, and applications in osteoporosis". Journal of Magnetic Resonance Imaging 33 (4): 974–979. April 2011. doi:10.1002/jmri.22489. PMID 21448966. 
  41. ↑ "Effects of estrogen therapy on bone marrow adipocytes in postmenopausal osteoporotic women". Osteoporosis International 19 (9): 1323–1330. September 2008. doi:10.1007/s00198-008-0574-6. PMID 18274695. 
  42. ↑ "Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment". Journal of Bone and Mineral Research 21 (1): 124–131. January 2006. doi:10.1359/jbmr.050916. PMID 16355281. 
  43. ↑ "Age-related changes in trabecular architecture differ in female and male C57BL/6J mice". Journal of Bone and Mineral Research 22 (8): 1197–1207. August 2007. doi:10.1359/jbmr.070507. PMID 17488199. 
  44. ↑ "Fat tissue, aging, and cellular senescence". Aging Cell 9 (5): 667–684. October 2010. doi:10.1111/j.1474-9726.2010.00608.x. PMID 20701600. 
  45. ↑ "Senescence-associated intrinsic mechanisms of osteoblast dysfunctions". Aging Cell 10 (2): 191–197. April 2011. doi:10.1111/j.1474-9726.2011.00669.x. PMID 21210937. 
  46. ↑ "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 (6): 379–389. December 2004. doi:10.1111/j.1474-9728.2004.00127.x. PMID 15569355. 
  47. ↑ "Wnt10b deficiency results in age-dependent loss of bone mass and progressive reduction of mesenchymal progenitor cells". Journal of Bone and Mineral Research 25 (10): 2138–2147. October 2010. doi:10.1002/jbmr.118. PMID 20499361. 
  48. ↑ "Wnt10b increases postnatal bone formation by enhancing osteoblast differentiation". Journal of Bone and Mineral Research 22 (12): 1924–1932. December 2007. doi:10.1359/jbmr.070810. PMID 17708715. 
  49. ↑ "Fate decision of mesenchymal stem cells: adipocytes or osteoblasts?". Cell Death and Differentiation 23 (7): 1128–1139. July 2016. doi:10.1038/cdd.2015.168. PMID 26868907. 
  50. ↑ "Bone marrow adipocytes promote the regeneration of stem cells and haematopoiesis by secreting SCF". Nature Cell Biology 19 (8): 891–903. August 2017. doi:10.1038/ncb3570. PMID 28714970. 
  51. ↑ "Short-term exposure to low-carbohydrate, high-fat diets induces low bone mineral density and reduces bone formation in rats". Journal of Bone and Mineral Research 25 (2): 275–284. February 2010. doi:10.1359/jbmr.090813. PMID 19653818. 
  52. ↑ "Sclerostin antibody inhibits skeletal deterioration due to reduced mechanical loading". Journal of Bone and Mineral Research 28 (4): 865–874. April 2013. doi:10.1002/jbmr.1807. PMID 23109229. 
  53. ↑ "Congenic mice with low serum IGF-I have increased body fat, reduced bone mineral density, and an altered osteoblast differentiation program". Bone 35 (5): 1046–1058. November 2004. doi:10.1016/j.bone.2004.07.008. PMID 15542029. 
  54. ↑ "Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment". Nature 460 (7252): 259–263. July 2009. doi:10.1038/nature08099. PMID 19516257. Bibcode: 2009Natur.460..259N. 
  55. ↑ "Mechanical loading down-regulates peroxisome proliferator-activated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis". Endocrinology 148 (5): 2553–2562. May 2007. doi:10.1210/en.2006-1704. PMID 17317771. 
  56. ↑ "Adipose lineage specification of bone marrow-derived myeloid cells". Adipocyte 1 (4): 215–229. October 2012. doi:10.4161/adip.21496. PMID 23700536. 
  57. ↑ "Analysis and Isolation of Adipocytes by Flow Cytometry". Methods of Adipose Tissue Biology, Part A. Methods in Enzymology. 537. 2014. pp. 281–96. doi:10.1016/b978-0-12-411619-1.00015-x. ISBN 9780124116191. 
  58. ↑ "Flow cytometric analysis of mature adipocytes". Cytometry 10 (4): 469–474. July 1989. doi:10.1002/cyto.990100416. PMID 2766892. 
  59. ↑ "Vertebral bone marrow fat is positively associated with visceral fat and inversely associated with IGF-1 in obese women". Obesity 19 (1): 49–53. January 2011. doi:10.1038/oby.2010.106. PMID 20467419. 
  60. ↑ "VDR haploinsufficiency impacts body composition and skeletal acquisition in a gender-specific manner". Calcified Tissue International 89 (3): 179–191. September 2011. doi:10.1007/s00223-011-9505-1. PMID 21637996. 
  61. ↑ "Marrow fat and preadipocyte factor-1 levels decrease with recovery in women with anorexia nervosa". Journal of Bone and Mineral Research 27 (9): 1864–1871. September 2012. doi:10.1002/jbmr.1640. PMID 22508185. 
  62. ↑ "Differential effects of exercise on tibial shaft marrow density in young female athletes". The Journal of Clinical Endocrinology and Metabolism 98 (5): 2037–2044. May 2013. doi:10.1210/jc.2012-3748. PMID 23616150. 
  63. ↑ "Use of Osmium Tetroxide Staining with Microcomputerized Tomography to Visualize and Quantify Bone Marrow Adipose Tissue in Vivo". Methods of Adipose Tissue Biology, Part A. Methods in Enzymology. 537. 2014. pp. 123–39. doi:10.1016/b978-0-12-411619-1.00007-0. ISBN 9780124116191. 
  64. ↑ "Human Bone Marrow Adipose Tissue is a Metabolically Active and Insulin-Sensitive Distinct Fat Depot". The Journal of Clinical Endocrinology and Metabolism 105 (7): 2300–2310. July 2020. doi:10.1210/clinem/dgaa216. PMID 32311037. 
  65. ↑ "The International Bone Marrow Adiposity Society". https://bma-society.org. 
  66. ↑ "Reporting Guidelines, Review of Methodological Standards, and Challenges Toward Harmonization in Bone Marrow Adiposity Research. Report of the Methodologies Working Group of the International Bone Marrow Adiposity Society". Frontiers in Endocrinology 11: 65. 2020. doi:10.3389/fendo.2020.00065. PMID 32180758. 
  67. ↑ "Guidelines for Biobanking of Bone Marrow Adipose Tissue and Related Cell Types: Report of the Biobanking Working Group of the International Bone Marrow Adiposity Society". Frontiers in Endocrinology 12: 744527. 2021. doi:10.3389/fendo.2021.744527. PMID 34646237. 
  68. ↑ "New insights into bone marrow adipocytes: Report from the First European Meeting on Bone Marrow Adiposity (BMA 2015)". Bone 93: 212–215. December 2016. doi:10.1016/j.bone.2015.11.013. PMID 26608519. 
  69. ↑ "Meeting report of the 2016 bone marrow adiposity meeting". Adipocyte 6 (4): 304–313. October 2017. doi:10.1080/21623945.2017.1313374. PMID 28410005. 
  70. ↑ "Brief Report From the 3rd International Meeting on Bone Marrow Adiposity (BMA 2017)". Frontiers in Endocrinology 10: 336. 2019. doi:10.3389/fendo.2019.00336. PMID 31191458. 
  71. ↑ "Brief Report From the 4th International Meeting on Bone Marrow Adiposity (BMA2018)". Frontiers in Endocrinology 10: 691. 2019. doi:10.3389/fendo.2019.00691. PMID 31681168. 
  72. ↑ "Report From the 6th International Meeting on Bone Marrow Adiposity (BMA2020)". Frontiers in Endocrinology 12: 712088. 2021. doi:10.3389/fendo.2021.712088. PMID 34335478. 
  73. ↑ "Next Generation Bone Marrow Adiposity Researchers: Report From the 1st BMAS Summer School 2021". Frontiers in Endocrinology 13: 879588. 2022. doi:10.3389/fendo.2022.879588. PMID 35498418. 

Further reading



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