Annals of the New York Academy of Sciences What's the Matter with Mat? Marrow Adipose Tissue, Metabolism, and Skeletal Health

Marrow adipose tissue (MAT) is functionally distinct from both white and brown adipose tissue and can contribute to systemic and skeletal metabolism. MAT formation is a spatially and temporally defined developmental event, suggesting that MAT is an organ that serves important functions and, like other organs, can undergo pathologic change. The well‐documented inverse relationship between MAT and bone mineral density has been interpreted to mean that MAT removal is a possible therapeutic target for osteoporosis. However, the bone and metabolic phenotypes of patients with lipodystrophy argues that retention of MAT may actually be beneficial in some circumstances. Furthermore, MAT may exist in two forms, regulated and constitutive, with divergent responses to hematopoietic and nutritional demands. In this review, we discuss the role of MAT in lipodystrophy, bone loss, and metabolism, and highlight our current understanding of this unique adipose tissue depot.

[1]  J. Laredo,et al.  Serous transformation of marrow of distal femoral epiphysis in a patient with congenital general lipodystrophy and spondylarthritis. , 2013, Joint, bone, spine : revue du rhumatisme.

[2]  Xiaojuan Li,et al.  Bone marrow fat composition as a novel imaging biomarker in postmenopausal women with prevalent fragility fractures , 2013, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[3]  Shixin Chang,et al.  The temporal characterization of marrow lipids and adipocytes in a rabbit model of glucocorticoid-induced osteoporosis , 2013, Skeletal Radiology.

[4]  M. Lathrop,et al.  Thiazolidinediones partially reverse the metabolic disturbances observed in Bscl2/seipin-deficient mice , 2013, Diabetologia.

[5]  O. MacDougald,et al.  Marrow fat and bone--new perspectives. , 2013, The Journal of clinical endocrinology and metabolism.

[6]  C. Rosen,et al.  New insights into osteoporosis: the bone–fat connection , 2012, Journal of internal medicine.

[7]  R. Müller,et al.  Increased marrow adiposity in premenopausal women with idiopathic osteoporosis. , 2012, The Journal of clinical endocrinology and metabolism.

[8]  S. Heymsfield,et al.  MRI-measured pelvic bone marrow adipose tissue is inversely related to DXA-measured bone mineral in younger and older Adults , 2012, European Journal of Clinical Nutrition.

[9]  B. Lecka-Czernik Marrow fat metabolism is linked to the systemic energy metabolism. , 2012, Bone.

[10]  Y. Lu,et al.  Bone marrow fat has brown adipose tissue characteristics, which are attenuated with aging and diabetes. , 2012, Bone.

[11]  Sean M. Hartig,et al.  Berardinelli-Seip Congenital Lipodystrophy 2/Seipin Is a Cell-Autonomous Regulator of Lipolysis Essential for Adipocyte Differentiation , 2012, Molecular and Cellular Biology.

[12]  S. Heymsfield,et al.  Ethnic and sex differences in bone marrow adipose tissue and bone mineral density relationship , 2012, Osteoporosis International.

[13]  S. O’Rahilly,et al.  Mechanistic insights into insulin resistance in the genetic era , 2011, Diabetic medicine : a journal of the British Diabetic Association.

[14]  M. Devlin Why does starvation make bones fat? , 2011, American journal of human biology : the official journal of the Human Biology Council.

[15]  Liping Zhao,et al.  Seipin ablation in mice results in severe generalized lipodystrophy. , 2011, Human molecular genetics.

[16]  F. Kraemer,et al.  Characterization of age-related gene expression profiling in bone marrow and epididymal adipocytes , 2011, BMC Genomics.

[17]  T. Clemens,et al.  The osteoblast: An insulin target cell controlling glucose homeostasis , 2011, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[18]  J. Cauley,et al.  The Role of Bone Marrow and Visceral Fat on Bone Metabolism , 2011, Current osteoporosis reports.

[19]  T. Wren,et al.  Bone marrow fat is inversely related to cortical bone in young and old subjects. , 2011, The Journal of clinical endocrinology and metabolism.

[20]  C. Rosen,et al.  Temperatures rising: brown fat and bone. , 2011, Discovery medicine.

[21]  R. Baron,et al.  Caloric restriction leads to high marrow adiposity and low bone mass in growing mice , 2010, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[22]  J. Dormans,et al.  Case Report: Unicameral Bone Cysts in a Young Patient with Acquired Generalized Lipodystrophy , 2010, Clinical orthopaedics and related research.

[23]  J. Chan,et al.  Rationale for leptin-replacement therapy for severe lipodystrophy. , 2010, Endocrine practice : official journal of the American College of Endocrinology and the American Association of Clinical Endocrinologists.

[24]  D. Seelow,et al.  Fatal Cardiac Arrhythmia and Long-QT Syndrome in a New Form of Congenital Generalized Lipodystrophy with Muscle Rippling (CGL4) Due to PTRF-CAVIN Mutations , 2010, PLoS genetics.

[25]  Cristina T Fonseca,et al.  Novel mutations of the BSCL2 and AGPAT2 genes in 10 families with Berardinelli–Seip congenital generalized lipodystrophy syndrome , 2009, Clinical endocrinology.

[26]  Keith L March,et al.  The human lipodystrophy gene product Berardinelli-Seip congenital lipodystrophy 2/seipin plays a key role in adipocyte differentiation. , 2009, Endocrinology.

[27]  I. Nonaka,et al.  Human PTRF mutations cause secondary deficiency of caveolins resulting in muscular dystrophy with generalized lipodystrophy. , 2009, The Journal of clinical investigation.

[28]  R. Hughson,et al.  Bone marrow fat accumulation after 60 days of bed rest persisted 1 year after activities were resumed along with hemopoietic stimulation: the Women International Space Simulation for Exploration study. , 2009, Journal of applied physiology.

[29]  M. Bredella,et al.  Increased bone marrow fat in anorexia nervosa. , 2009, The Journal of clinical endocrinology and metabolism.

[30]  A. Klibanski,et al.  Bone, fat, and body composition: evolving concepts in the pathogenesis of osteoporosis. , 2009, The American journal of medicine.

[31]  G. Daley,et al.  Bone marrow adipocytes as negative regulators of the hematopoietic microenvironment , 2009, Nature.

[32]  A. K. Agarwal,et al.  Molecular mechanisms of hepatic steatosis and insulin resistance in the AGPAT2-deficient mouse model of congenital generalized lipodystrophy. , 2009, Cell metabolism.

[33]  H. Aytan,et al.  Is leptin a significant predictor of bone mineral density in postmenopausal Turkish women? , 2009, Rheumatology International.

[34]  K. H. Albrecht,et al.  Deletion of Cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. , 2008, Cell metabolism.

[35]  L. Maldergem,et al.  Congenital generalized lipodystrophy in an Indian patient with a novel mutation in BSCL2 gene , 2008, Journal of Inherited Metabolic Disease.

[36]  S. O’Rahilly,et al.  Association of a homozygous nonsense caveolin-1 mutation with Berardinelli-Seip congenital lipodystrophy. , 2008, The Journal of clinical endocrinology and metabolism.

[37]  S. Kanazawa,et al.  Computed tomography findings of congenital generalized lipodystrophy: multiple nodular fatty liver and diffuse sclerosis of bones , 2007, Radiation Medicine.

[38]  F. Bandeira,et al.  High bone mass associated with berardinelli lipodystrophy. , 2007, Endocrine practice : official journal of the American College of Endocrinology and the American Association of Clinical Endocrinologists.

[39]  H. Jo,et al.  Caveolin‐1 Knockout Mice Have Increased Bone Size and Stiffness , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[40]  S. B. Heymsfield,et al.  MRI-measured bone marrow adipose tissue is inversely related to DXA-measured bone mineral in Caucasian women , 2007, Osteoporosis International.

[41]  D. Mellström,et al.  Leptin Is a Negative Independent Predictor of Areal BMD and Cortical Bone Size in Young Adult Swedish Men , 2006, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[42]  O. MacDougald,et al.  Adipocyte differentiation from the inside out , 2006, Nature Reviews Molecular Cell Biology.

[43]  M. Hamrick,et al.  Injections of leptin into rat ventromedial hypothalamus increase adipocyte apoptosis in peripheral fat and in bone marrow , 2006, Cell and Tissue Research.

[44]  E. Barrett-Connor,et al.  Leptin Predicts BMD and Bone Resorption in Older Women but Not Older Men: The Rancho Bernardo Study , 2006, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[45]  W. Jee,et al.  Variations in mineral apposition rate of trabecular bone within the beagle skeleton , 2006, Calcified Tissue International.

[46]  Ping Chung Leung,et al.  Vertebral bone mineral density, marrow perfusion, and fat content in healthy men and men with osteoporosis: dynamic contrast-enhanced MR imaging and MR spectroscopy. , 2005, Radiology.

[47]  M. Hamrick,et al.  Novel treatments for obesity and osteoporosis: targeting apoptotic pathways in adipocytes. , 2005, Current medicinal chemistry.

[48]  J. Woo,et al.  Osteoporosis is associated with increased marrow fat content and decreased marrow fat unsaturation: A proton MR spectroscopy study , 2005, Journal of magnetic resonance imaging : JMRI.

[49]  S. Chanprasertyothin,et al.  Association of circulating leptin with bone mineral density in males and females. , 2005, Journal of the Medical Association of Thailand = Chotmaihet thangphaet.

[50]  Üçler Kısa,et al.  Plasma Leptin Concentrations in Postmenopausal Women with Osteoporosis , 2005, Endocrine research.

[51]  M. Tavassoli Differential response of bone marrow and extramedullary adipose cells to starvation , 1974, Experientia.

[52]  H. Xie,et al.  Relationship of serum leptin with age, body weight, body mass index, and bone mineral density in healthy mainland Chinese women. , 2005, Clinica chimica acta; international journal of clinical chemistry.

[53]  M. Lisanti,et al.  Role of caveolae and caveolins in health and disease. , 2004, Physiological reviews.

[54]  T. Tai,et al.  Lack of independent relationship between plasma adiponectin, leptin levels and bone density in nondiabetic female adolescents , 2004, Clinical endocrinology.

[55]  A. Shuldiner,et al.  Mutations in Gng3lg and AGPAT2 in Berardinelli-Seip congenital lipodystrophy and Brunzell syndrome: phenotype variability suggests important modifier effects. , 2004, The Journal of clinical endocrinology and metabolism.

[56]  P. Gorden,et al.  Changes in body composition in patients with severe lipodystrophy after leptin replacement therapy. , 2004, Metabolism: clinical and experimental.

[57]  J. Seckl,et al.  Mice deficient in 11beta-hydroxysteroid dehydrogenase type 1 lack bone marrow adipocytes, but maintain normal bone formation. , 2004, Endocrinology.

[58]  M. Tavassoli,et al.  Retention of hemopoiesis in tail vertebrae of newborn rats , 1979, Cell and Tissue Research.

[59]  M. Tavassoli,et al.  Studies on bone marrow histogenesis: Morphometric and autoradiographic studies of regenerating marrow stroma in extramedullary autoimplants and after evacuation of marrow cavity , 1978, Cell and Tissue Research.

[60]  R. Peshock,et al.  The skeleton in congenital, generalized lipodystrophy: evaluation using whole-body radiographic surveys, magnetic resonance imaging and technetium-99m bone scintigraphy , 2004, Skeletal Radiology.

[61]  D. Sartoris,et al.  Case report 417 , 2004, Skeletal Radiology.

[62]  M. Kricun Red-yellow marrow conversion: Its effect on the location of some solitary bone lesions , 2004, Skeletal Radiology.

[63]  Jan Nedergaard,et al.  Brown adipose tissue: function and physiological significance. , 2004, Physiological reviews.

[64]  O. Pedersen,et al.  Leptin and bone mineral density: a cross-sectional study in obese and nonobese men. , 2003, The Journal of clinical endocrinology and metabolism.

[65]  A. Garg,et al.  Phenotypic heterogeneity in body fat distribution in patients with congenital generalized lipodystrophy caused by mutations in the AGPAT2 or seipin genes. , 2003, The Journal of clinical endocrinology and metabolism.

[66]  R. Porcher,et al.  Serum leptin as a determinant of bone resorption in healthy postmenopausal women. , 2003, Bone.

[67]  S. Heymsfield,et al.  Relationship of leptin and sex hormones to bone mineral density in men , 2003, Acta Diabetologica.

[68]  R. Vettor,et al.  Relationship between leptin levels and bone mineral density in the elderly , 2003, Clinical endocrinology.

[69]  A. Garg,et al.  Congenital generalized lipodystrophy: significance of triglyceride biosynthetic pathways , 2003, Trends in Endocrinology & Metabolism.

[70]  M. Lathrop,et al.  Prevalence of mutations in AGPAT2 among human lipodystrophies. , 2003, Diabetes.

[71]  C. Mantzoros,et al.  Relationship of leptin to bone mineralization in children and adolescents. , 2003, The Journal of clinical endocrinology and metabolism.

[72]  T. Ushiroyama,et al.  Inverse correlation between serum leptin concentration and vertebral bone density in postmenopausal women , 2003, Gynecological endocrinology : the official journal of the International Society of Gynecological Endocrinology.

[73]  Y. Matsuzawa,et al.  Serum adiponectin and leptin levels in patients with lipodystrophies. , 2004, The Journal of clinical endocrinology and metabolism.

[74]  H. Syddall,et al.  Plasma Leptin Concentration and Change in Bone Density Among Elderly Men and Women: The Hertfordshire Cohort Study , 2004, Calcified Tissue International.

[75]  G. Polat,et al.  Body composition, bone mineral density, and circulating leptin levels in postmenopausal Turkish women , 2003, Rheumatology International.

[76]  J. Zerwekh,et al.  Effect of subcutaneous leptin replacement therapy on bone metabolism in patients with generalized lipodystrophy. , 2002, The Journal of clinical endocrinology and metabolism.

[77]  Patricia Ducy,et al.  Leptin Regulates Bone Formation via the Sympathetic Nervous System , 2002, Cell.

[78]  J. Everhart,et al.  Relationship of Serum Leptin Concentration With Bone Mineral Density in the United States Population , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[79]  M. Patton,et al.  Heterogeneity for congenital generalized lipodystrophy in seventeen patients from Oman. , 2002, American journal of medical genetics.

[80]  David S. Park,et al.  Caveolin-1-deficient Mice Are Lean, Resistant to Diet-induced Obesity, and Show Hypertriglyceridemia with Adipocyte Abnormalities* , 2002, The Journal of Biological Chemistry.

[81]  Simeon I. Taylor,et al.  Lipoatrophic-lipodystrophic syndromes: the spectrum of findings on MR imaging. , 2002, AJR. American journal of roentgenology.

[82]  K. Yasuda,et al.  Association between serum leptin concentrations and bone mineral density, and biochemical markers of bone turnover in adult men. , 2001, The Journal of clinical endocrinology and metabolism.

[83]  K. Chihara,et al.  Plasma leptin concentrations are associated with bone mineral density and the presence of vertebral fractures in postmenopausal women , 2001, Clinical endocrinology.

[84]  L. Melton,et al.  Role of serum leptin, insulin, and estrogen levels as potential mediators of the relationship between fat mass and bone mineral density in men versus women. , 2001, Bone.

[85]  Y. Terauchi,et al.  The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity , 2001, Nature Medicine.

[86]  E. Falk,et al.  Troglitazone Treatment Increases Bone Marrow Adipose Tissue Volume but Does not Affect Trabecular Bone Volume in Mice , 2001, Calcified Tissue International.

[87]  J. Pasco,et al.  Serum leptin levels are associated with bone mass in nonobese women. , 2001, The Journal of clinical endocrinology and metabolism.

[88]  T. Wronski,et al.  Decreased bone anabolic effect of basic fibroblast growth factor at fatty marrow sites in ovariectomized rats. , 2001, Bone.

[89]  R. Nuti,et al.  Influence of insulin-like growth factor-1 and leptin on bone mass in healthy postmenopausal women. , 2001, Bone.

[90]  I. Maruyama,et al.  A possible role for leptin in normo- or hypoparathyroid uremic bone in postmenopausal dialysis women , 2001, Journal of Bone and Mineral Metabolism.

[91]  D. Dunger,et al.  Increased Bone Mineral Density and Serum Leptin in Non-Obese Girls with Precocious Pubarche: Relation to Low Birthweight and Hyperinsulinism , 2001, Hormone Research in Paediatrics.

[92]  R. Pacifici,et al.  Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. , 2000, The Journal of clinical investigation.

[93]  Arndt F Schilling,et al.  Leptin Inhibits Bone Formation through a Hypothalamic Relay A Central Control of Bone Mass , 2000, Cell.

[94]  R. Hammer,et al.  Leptin reverses insulin resistance and diabetes mellitus in mice with congenital lipodystrophy , 1999, Nature.

[95]  Y. Tamura,et al.  Histomorphometric Evaluation of the Effects of Ovariectomy on Bone Turnover in Rat Caudal Vertebrae , 1999, Calcified Tissue International.

[96]  T. Wronski,et al.  Parathyroid hormone stimulates cancellous bone formation at skeletal sites regardless of marrow composition in ovariectomized rats. , 1999, Bone.

[97]  N. Harada,et al.  Aromatase in Human Bone Tissue , 1997, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[98]  T. Wronski,et al.  Comparative study of skeletal response to estrogen depletion at red and yellow marrow sites in rats , 1996, The Anatomical record.

[99]  O. Trygstad,et al.  Generalized lipodystrophy, congenital and acquired (lipoatrophy) , 1996, Acta paediatrica (Oslo, Norway : 1992). Supplement.

[100]  J. Westvik Radiological features in generalized lipodystrophy , 1996, Acta paediatrica (Oslo, Norway : 1992). Supplement.

[101]  B. Maldague,et al.  Distribution of serouslike bone marrow changes in the lower limbs of patients with anorexia nervosa: predominant involvement of the distal extremities. , 1996, AJR. American journal of roentgenology.

[102]  H. Robins,et al.  Canine bone marrow as a potential thermal sanctuary during the plateau phase of 41.8°C whole body hyperthermia , 1995 .

[103]  H. Robins,et al.  Canine bone marrow as a potential thermal sanctuary during the plateau phase of 41.8 degrees C whole body hyperthermia. , 1995, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[104]  S. Grundy,et al.  Peculiar distribution of adipose tissue in patients with congenital generalized lipodystrophy. , 1992, The Journal of clinical endocrinology and metabolism.

[105]  F. Shellock,et al.  Hematopoietic bone marrow hyperplasia: high prevalence on MR images of the knee in asymptomatic marathon runners. , 1992, AJR. American journal of roentgenology.

[106]  R. Martin,et al.  Relationships between marrow fat and bone turnover in ovariectomized and intact rats. , 1991, Bone.

[107]  D. Caramella,et al.  Hematopoietic bone marrow recovery after radiation therapy: MRI evaluation. , 1989, Blood.

[108]  D. Sartoris,et al.  Case report 417: Lipoatrophic diabetes mellitus (generalized lipodystrophy). , 1987, Skeletal radiology.

[109]  W Eisenmenger,et al.  Changes in trabecular bone, hematopoiesis and bone marrow vessels in aplastic anemia, primary osteoporosis, and old age: a comparative histomorphometric study. , 1987, Bone.

[110]  M. Tavassoli,et al.  Fatty involution of bone marrow in rabbits. , 1984, Acta anatomica.

[111]  J. Canick,et al.  Human fatty marrow aromatizes androgen to estrogen. , 1980, The Journal of clinical endocrinology and metabolism.

[112]  M. Tavassoli Marrow adipose cells. Histochemical identification of labile and stable components. , 1976, Archives of pathology & laboratory medicine.

[113]  M. Tavassoli Ultrastructural development of bone marrow adipose cell. , 1976, Acta anatomica.

[114]  J. R. Güell-González,et al.  Bone lesions in congenital generalised lipodystrophy. , 1971, Lancet.

[115]  M. Tavassoli,et al.  Factors affecting the conversion of yellow to red marrow. , 1971, Blood.

[116]  M. Tavassoli,et al.  Bone Marrow Histogenesis: A Comparison of Fatty and Red Marrow , 1970, Science.

[117]  J. Brunzell,et al.  Congenital generalized lipodystrophy accompanied by cystic angiomatosis. , 1968, Annals of internal medicine.

[118]  J. Gwinn,et al.  The roentgenographic findings in total lipodystrophy. , 1968, The American journal of roentgenology, radium therapy, and nuclear medicine.

[119]  R. Gold,et al.  Lipoatrophic diabetes mellitus (generalized lipodystrophy): roentgen findings in two brothers with congenital disease. , 1967, The American journal of roentgenology, radium therapy, and nuclear medicine.

[120]  E. Shafrir,et al.  Yellow Bone Marrow as Adipose Tissue , 1967, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[121]  N. Petrakis Some physiological and developmental considerations of the temperature-gradient hypothesis of bone marrow distribution. , 1966, American journal of physical anthropology.

[122]  R. Wright,et al.  EFFECT OF LOCALIZED IRRADIATION ON THE METABOLISM OF BONE-MARROW LIPIDS. , 1965, Radiation research.

[123]  W. Reed,et al.  CONGENITAL LIPODYSTROPHIC DIABETES WITH ACANTHOSIS NIGRICANS: THE SEIP-LAWRENCE SYNDROME. , 1965, Archives of Dermatology.

[124]  F. Gardner,et al.  EFFECT OF MASSIVE TRIAMCINOLONE ADMINISTRATION IN BLUNTING THE ERYTHROPOIETIC RESPONSE TO PHENYLHYDRAZINE HEMOLYSIS. , 1965, The Journal of laboratory and clinical medicine.

[125]  J. Emery,et al.  Regression of Bone‐Marrow Haemopoiesis from the Terminal Digits in the Foetus and Infant , 1964, British journal of haematology.

[126]  B. Senior,et al.  THE SYNDROMES OF TOTAL LIPODYSTROPHY AND OF PARTIAL LIPODYSTROPHY. , 1964, Pediatrics.

[127]  O. Trygstad,et al.  Generalized lipodystrophy. , 2020, Ergebnisse der inneren Medizin und Kinderheilkunde.

[128]  I. Mcquarrie,et al.  Lipohistiodiaresis: a syndrome of lipodystrophy universalis, accelerated growth, lipemia, hepatic cirrhosis, and insulin-resistant diabetes without ketosis. , 1961, The Journal-lancet.

[129]  B. Senior Lipodystrophic Muscular Hypertrophy , 1961, Archives of disease in childhood.

[130]  A. Renold,et al.  Generalized lipoatrophy, hepatic cirrhosis, disturbed carbohydrate metabolism and accelerated growth (lipoatrophic diabetes). Longitudinal observations and metabolic studies. , 1960, The American journal of medicine.

[131]  M. Seip Lipodystrophy and gigantism with associated endocrine manifestations. A new diencephalic syndrome? , 1959, Acta paediatrica.

[132]  M. Seip 38. Congenital Hyperpituitarism of Hypothalamic Origin; A new Diencephalic Syndrome with Endocrine Manifestations , 1959, Acta paediatrica. Supplementum.

[133]  H. A. Meineke Lack of Hematopoiesis in Tail Bones Transposed to Abdominal Cavity of Hypophysectomized Rats.∗ , 1956, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[134]  J. Arneaud,et al.  A Case of True Hermaphroditism , 1956, British medical journal.

[135]  Spitzer Jj,et al.  Hemorrhagic lipemia: a derangement of fat metabolism. , 1955 .

[136]  J. Spitzer,et al.  Hemorrhagic lipemia: a derangement of fat metabolism. , 1955, The Journal of laboratory and clinical medicine.

[137]  W. Berardinelli An undiagnosed endocrinometabolic syndrome: report of 2 cases. , 1954, The Journal of clinical endocrinology and metabolism.

[138]  N. Petrakis Temperature of human bone marrow. , 1952, Journal of applied physiology.

[139]  J. Shillingford The Red Bone Marrow in Heart Failure , 1950, Journal of clinical pathology.

[140]  Newlin He,et al.  Bone marrow for fat storage in rabbits. , 1948 .

[141]  C. Mccay,et al.  Bone marrow for fat storage in rabbits. , 1948, Archives of biochemistry.

[142]  C. Huggins,et al.  CHANGES IN OUTLYING BONE MARROW ACCOMPANYING A LOCAL INCREASE OF TEMPERATURE WITHIN PHYSIOLOGICAL LIMITS , 1936, The Journal of experimental medicine.

[143]  G. Whipple,et al.  MARROW HYPERPLASIA AND HEMOGLOBIN RESERVE IN EXPERIMENTAL ANEMIA DUE TO BLEEDING , 1932, The Journal of experimental medicine.

[144]  R. Custer,et al.  Studies on the structure and function of bone marrow , 1932 .

[145]  A. Prenant,et al.  Traité d'histologie / , 1904 .