Advertisement

Calcified Tissue International

, Volume 100, Issue 5, pp 461–475 | Cite as

Evolution of the Marrow Adipose Tissue Microenvironment

  • Clarissa S. Craft
  • Erica L. Scheller
Review

Abstract

Adipocytes of the marrow adipose tissue (MAT) are distributed throughout the skeleton, are embedded in extracellular matrix, and are surrounded by cells of the hematopoietic and osteogenic lineages. MAT is a persistent component of the skeletal microenvironment and has the potential to impact local processes including bone accrual and hematopoietic function. In this review, we discuss the initial evolution of MAT in vertebrate lineages while emphasizing comparisons to the development of peripheral adipose, hematopoietic, and skeletal tissues. We then apply these evolutionary clues to define putative functions of MAT. Lastly, we explore the regulation of MAT by two major components of its microenvironment, the extracellular matrix and the nerves embedded within. The extracellular matrix and nerves contribute to both rapid and continuous modification of the MAT niche and may help to explain evolutionary conserved mechanisms underlying the coordinated regulation of blood, bone, and MAT within the skeleton.

Keywords

Evolution Marrow fat Bone Adipose Marrow adipose tissue Matrix 

Notes

Acknowledgments

This work was supported by the National Institutes of Health (K99/R00-DE024178 to E.L.S.), the American Diabetes Association (7-13-JF-16 to C.S.C.), and Washington University’s Musculoskeletal Research Center (JIT2014_Craft_1 to C.S.C.).

Conflict of Interest

Clarissa S. Craft and Erica L. Scheller declare that they have no conflict of interest.

References

  1. 1.
    Adler BJ, Kaushansky K, Rubin CT (2014) Obesity-driven disruption of haematopoiesis and the bone marrow niche. Nat Rev Endocrinol 10:737–748. doi: 10.1038/nrendo.2014.169 PubMedCrossRefGoogle Scholar
  2. 2.
    Schwartz AV (2015) Marrow fat and bone: review of clinical findings. Front Endocrinol (Lausanne) 6:40. doi: 10.3389/fendo.2015.00040 Google Scholar
  3. 3.
    Scheller EL, Rosen CJ (2014) What’s the matter with MAT? marrow adipose tissue, metabolism, and skeletal health. Ann N Y Acad Sci 1311:14–30. doi: 10.1111/nyas.12327 PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Scheller EL, Doucette CR, Learman BS et al (2015) Region-specific variation in the properties of skeletal adipocytes reveals regulated and constitutive marrow adipose tissues. Nat Commun 6:7808. doi: 10.1038/ncomms8808 PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Tavassoli M (1976) Marrow adipose cells. histochemical identification of labile and stable components. Arch Pathol Lab Med 100:16–18PubMedGoogle Scholar
  6. 6.
    Naveiras O, Nardi V, Wenzel PL et al (2009) Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 460:259–263. doi: 10.1038/nature08099 PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Scheller EL, Cawthorn WP, Burr AA et al (2016) Marrow adipose tissue: trimming the fat. Trends Endocrinol Metab. doi: 10.1016/j.tem.2016.03.016 PubMedGoogle Scholar
  8. 8.
    Patsch JM, Li X, Baum T et al (2013) Bone marrow fat composition as a novel imaging biomarker in postmenopausal women with prevalent fragility fractures. J Bone Miner Res 28:1721–1728. doi: 10.1002/jbmr.1950 PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Trudel G, Payne M, Mädler B et al (2009) 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. J Appl Physiol 107:540–548. doi: 10.1152/japplphysiol.91530.2008 PubMedCrossRefGoogle Scholar
  10. 10.
    Casamassima F, Ruggiero C, Caramella D et al (1989) Hematopoietic bone marrow recovery after radiation therapy: MRI evaluation. Blood 73:1677–1681PubMedGoogle Scholar
  11. 11.
    Boehm T, Hess I, Swann JB (2012) Evolution of lymphoid tissues. Trends Immunol 33:315–321. doi: 10.1016/j.it.2012.02.005 PubMedCrossRefGoogle Scholar
  12. 12.
    Pond CM (2012) The evolution of mammalian adipose tissue. In: Symonds ME (ed) Adipose tissue biology. Springer New York, New York, pp 227–269CrossRefGoogle Scholar
  13. 13.
    Vague J, Fenasse R (2010) Comparative anatomy of adipose tissue. Compr Physiol. doi: 10.1002/cphy.cp050105 Google Scholar
  14. 14.
    Gesta S, Tseng YH, Kahn CR (2007) Developmental origin of fat: tracking obesity to its source. Cell 131:242–256. doi: 10.1016/j.cell.2007.10.004 PubMedCrossRefGoogle Scholar
  15. 15.
    Hirasawa T, Kuratani S (2015) Evolution of the vertebrate skeleton: morphology, embryology, and development. Zool Lett 1:2. doi: 10.1186/s40851-014-0007-7 CrossRefGoogle Scholar
  16. 16.
    Raison RL, dos Remedios NJ (1998) The hagfish immune system. The Biology of Hagfishes. Springer, Netherlands, pp 334–344Google Scholar
  17. 17.
    Wagner DO, Aspenberg P (2011) Where did bone come from? Acta Orthop 82:393–398. doi: 10.3109/17453674.2011.588861 PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Amemiya CT, Saha NR, Zapata A (2007) Evolution and development of immunological structures in the lamprey. Curr Opin Immunol 19:535–541. doi: 10.1016/j.coi.2007.08.003 PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Histology and Morphology Of The Epigonal Organ With Special Reference To The Lymphomyeloid System In Rhinobatos rhinobatos. https://www.researchgate.net/publication/257307727_Histology_and_Morphology_Of_The_Epigonal_Organ_With_Special_Reference_To_The_Lymphomyeloid_System_In_Rhinobatos_rhinobatos. Accessed 9 May 2016
  20. 20.
    Walsh CJ, Luer CA (2004) Elasmobranch hematology: identification of cell types and practical applications. In: Smith M, Warmolts D, Thoney D, Hueter R (eds) Elasmobranch husbandry manual. Ohio Biological Survey Inc, Columbus, pp 307–323Google Scholar
  21. 21.
    Bennett CM, Kanki JP, Rhodes J et al (2001) Myelopoiesis in the zebrafish, danio rerio. Blood 98:643–651PubMedCrossRefGoogle Scholar
  22. 22.
    Ma D, Zhang J, Lin HF et al (2011) The identification and characterization of zebrafish hematopoietic stem cells. Blood 118:289–297. doi: 10.1182/blood-2010-12-327403 PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Witten PE, Hansen A, Hall BK (2001) Features of mono- and multinucleated bone resorbing cells of the zebrafish danio rerio and their contribution to skeletal development, remodeling, and growth. J Morphol 250:197–207. doi: 10.1002/jmor.1065 PubMedCrossRefGoogle Scholar
  24. 24.
    Tavassoli M (1986) Bone marrow in boneless fish: lessons of evolution. Med Hypotheses 20:9–15. doi: 10.1016/0306-9877(86)90081-2 PubMedCrossRefGoogle Scholar
  25. 25.
    Scharrer E (1944) The histology of the meningeal myeloid tissue in the ganoids amia and lepisosteus. Anat Rec 88:291–310. doi: 10.1002/ar.1090880307 CrossRefGoogle Scholar
  26. 26.
    Genten F, Terwinghe E, Danguy A (2009) Atlas of fish histology, hardcover; 2009-01-01. Science Publishers, EnfieldGoogle Scholar
  27. 27.
    Curtis SK, Cowden RR, Nagel JW (1979) Ultrastructure of the bone marrow of the salamander plethodon glutinosus (Caudata: plethodontidae). J Morphol 159:151–183. doi: 10.1002/jmor.1051590202 CrossRefGoogle Scholar
  28. 28.
    Hightower JA, Pierre RLS (1971) Hemopoietic tissue in the adult newt, Notopthalmus viridescens. J Morphol 135:299–307. doi: 10.1002/jmor.1051350304 CrossRefGoogle Scholar
  29. 29.
    Jordan HE (1919) The histology of the blood and the red bone-marrow of the leopard frog, rana pipiens. Am J Anat 25:436–480. doi: 10.1002/aja.1000250404 CrossRefGoogle Scholar
  30. 30.
    Wells KD (2010) The ecology and behavior of amphibians. University of Chicago Press, ChicagoGoogle Scholar
  31. 31.
    Cawthorn WP, Scheller EL, Learman BS et al (2014) Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction. Cell Metab 20:368–375. doi: 10.1016/j.cmet.2014.06.003 PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Devlin MJ, Cloutier AM, Thomas NA et al (2010) Caloric restriction leads to high marrow adiposity and low bone mass in growing mice. J Bone Miner Res 25:2078–2088. doi: 10.1002/jbmr.82 PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Werner YL (1971) The ontogenic development of the vertebrae in some gekkonoid lizards. J Morphol 133:41–91. doi: 10.1002/jmor.1051330104 PubMedCrossRefGoogle Scholar
  34. 34.
    Zapata A, Leceta J, Villena A (1981) Reptilian bone marrow. an ultrastructural study in the spanish lizard. Lacerta hispanica. J Morphol 168:137–149. doi: 10.1002/jmor.1051680203 Google Scholar
  35. 35.
    Campbell F (1967) Fine structure of the bone marrow of the chicken and pigeon. J Morphol 123:405–439. doi: 10.1002/jmor.1051230407 PubMedCrossRefGoogle Scholar
  36. 36.
    Li SC, Lin CY, Kuo TF et al (2010) Chicken model of steroid-induced bone marrow adipogenesis using proteome analysis: a preliminary study. Proteome Sci 8:47. doi: 10.1186/1477-5956-8-47 PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Cawthorn WP, Scheller EL, Parlee SD et al (2016) Expansion of bone marrow adipose tissue during caloric restriction is associated with increased circulating glucocorticoids and not with hypoleptinemia. Endocrinology 157:508–521. doi: 10.1210/en.2015-1477 PubMedCrossRefGoogle Scholar
  38. 38.
    Bigelow CL, Tavassoli M (1984) Fatty involution of bone marrow in rabbits. Acta Anat (Basel) 118:60–64CrossRefGoogle Scholar
  39. 39.
    Bigelow CL, Tavassoli M (1984) Studies on conversion of yellow marrow to red marrow by using ectopic bone marrow implants. Exp Hematol 12:581–585PubMedGoogle Scholar
  40. 40.
    Tavassoli M, Crosby WH (1970) Bone marrow histogenesis: a comparison of fatty and red marrow. Science 169:291–293PubMedCrossRefGoogle Scholar
  41. 41.
    Weiss LP, Wislocki GB (1956) Seasonal variations in hematopoiesis in the dermal bones of the nine-banded armadillo. Anat Rec 126:143–163PubMedCrossRefGoogle Scholar
  42. 42.
    Hill RV (2006) Comparative anatomy and histology of xenarthran osteoderms. J Morphol 267:1441–1460. doi: 10.1002/jmor.10490 PubMedCrossRefGoogle Scholar
  43. 43.
    Li GW, Xu Z, Chen QW et al (2013) The temporal characterization of marrow lipids and adipocytes in a rabbit model of glucocorticoid-induced osteoporosis. Skeletal Radiol 42:1235–1244. doi: 10.1007/s00256-013-1659-7 PubMedCrossRefGoogle Scholar
  44. 44.
    Hamrick MW, Della Fera MA, Choi YH et al (2007) Injections of leptin into rat ventromedial hypothalamus increase adipocyte apoptosis in peripheral fat and in bone marrow. Cell Tissue Res 327:133–141. doi: 10.1007/s00441-006-0312-3 PubMedCrossRefGoogle Scholar
  45. 45.
    Ma HT, Ren R, Chen Y et al (2014) A simulation study of marrow fat effect on bone biomechanics. Conf Proc IEEE Eng Med Biol Soc 2014:4030–4033. doi: 10.1109/EMBC.2014.6944508 PubMedGoogle Scholar
  46. 46.
    Gunaratnam K, Vidal C, Gimble JM, Duque G (2014) Mechanisms of palmitate-induced lipotoxicity in human osteoblasts. Endocrinology 155:108–116. doi: 10.1210/en.2013-1712 PubMedCrossRefGoogle Scholar
  47. 47.
    Hardaway AL, Herroon MK, Rajagurubandara E, Podgorski I (2015) Marrow adipocyte-derived CXCL1 and CXCL2 contribute to osteolysis in metastatic prostate cancer. Clin Exp Metastasis 32:353–368. doi: 10.1007/s10585-015-9714-5 PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Mattacks CA, Pond CM (1999) Interactions of noradrenalin and tumour necrosis factor alpha, interleukin 4 and interleukin 6 in the control of lipolysis from adipocytes around lymph nodes. Cytokine 11:334–346. doi: 10.1006/cyto.1998.0442 PubMedCrossRefGoogle Scholar
  49. 49.
    MacQueen HA, Pond CM (1998) Immunofluorescent localisation of tumour necrosis factor-alpha receptors on the popliteal lymph node and the surrounding adipose tissue following a simulated immune challenge. J Anat 192(Pt 2):223–231PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Pond CM, Mattacks CA (2003) The source of fatty acids incorporated into proliferating lymphoid cells in immune-stimulated lymph nodes. Br J Nutr 89:375–383. doi: 10.1079/BJN2002784 PubMedCrossRefGoogle Scholar
  51. 51.
    Pond CM (2007) Interactions of adipose and lymphoid tissues. In: Fantuzzi G, Mazzone T (eds) Adipose tissue and adipokines in health and disease. Humana Press, Totowa, pp 133–150CrossRefGoogle Scholar
  52. 52.
    Adamo SA, Bartlett A, Le J et al (2010) Illness-induced anorexia may reduce trade-offs between digestion and immune function. Anim Behav 79:3–10. doi: 10.1016/j.anbehav.2009.10.012 CrossRefGoogle Scholar
  53. 53.
    Johnson RW (2002) The concept of sickness behavior: a brief chronological account of four key discoveries. Vet Immunol Immunopathol 87:443–450PubMedCrossRefGoogle Scholar
  54. 54.
    Straub RH, Cutolo M, Buttgereit F, Pongratz G (2010) Energy regulation and neuroendocrine-immune control in chronic inflammatory diseases. J Intern Med 267:543–560. doi: 10.1111/j.1365-2796.2010.02218.x PubMedCrossRefGoogle Scholar
  55. 55.
    Adams JC (2013) Extracellular matrix evolution: an overview. In: Keeley FW, Mecham RP (eds) Evolution of extracellular matrix. Springer, New York, pp 1–25CrossRefGoogle Scholar
  56. 56.
    Klein G, Müller CA, Tillet E et al (1995) Collagen type VI in the human bone marrow microenvironment: a strong cytoadhesive component. Blood 86:1740–1748PubMedGoogle Scholar
  57. 57.
    Nilsson SK, Debatis ME, Dooner MS et al (1998) Immunofluorescence characterization of key extracellular matrix proteins in murine bone marrow in situ. J Histochem Cytochem 46:371–377PubMedCrossRefGoogle Scholar
  58. 58.
    Malara A, Currao M, Gruppi C et al (2014) Megakaryocytes contribute to the bone marrow-matrix environment by expressing fibronectin, type IV collagen, and laminin. Stem Cells 32:926–937. doi: 10.1002/stem.1626 PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Carter DH, Sloan P, Aaron JE (1991) Immunolocalization of collagen types I and III, tenascin, and fibronectin in intramembranous bone. J Histochem Cytochem 39:599–606PubMedCrossRefGoogle Scholar
  60. 60.
    Hamilton R, Campbell FR (1991) Immunochemical localization of extracellular materials in bone marrow of rats. Anat Rec 231:218–224. doi: 10.1002/ar.1092310210 PubMedCrossRefGoogle Scholar
  61. 61.
    Khan T, Muise ES, Iyengar P et al (2009) Metabolic dysregulation and adipose tissue fibrosis: role of collagen VI. Mol Cell Biol 29:1575–1591. doi: 10.1128/MCB.01300-08 PubMedCrossRefGoogle Scholar
  62. 62.
    Nakamura-Ishizu A, Okuno Y, Omatsu Y et al (2012) Extracellular matrix protein tenascin-C is required in the bone marrow microenvironment primed for hematopoietic regeneration. Blood 119:5429–5437. doi: 10.1182/blood-2011-11-393645 PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Campell AD, Long MW, Wicha MS (1987) Haemonectin, a bone marrow adhesion protein specific for cells of granulocyte lineage. Nature 329:744–746CrossRefGoogle Scholar
  64. 64.
    Smaldone S, Clayton NP, Del Solar M et al (2016) Fibrillin-1 regulates skeletal stem cell differentiation by modulating TGFβ activity within the marrow niche. J Bone Miner Res 31:86–97. doi: 10.1002/jbmr.2598 PubMedCrossRefGoogle Scholar
  65. 65.
    Mori S, Kiuchi S, Ouchi A et al (2014) Characteristic expression of extracellular matrix in subcutaneous adipose tissue development and adipogenesis; comparison with visceral adipose tissue. Int J Biol Sci 10:825–833. doi: 10.7150/ijbs.8672 PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Sun K, Tordjman J, Clément K, Scherer PE (2013) Fibrosis and adipose tissue dysfunction. Cell Metab 18:470–477. doi: 10.1016/j.cmet.2013.06.016 PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Alford AI, Hankenson KD (2006) Matricellular proteins: extracellular modulators of bone development, remodeling, and regeneration. Bone 38:749–757. doi: 10.1016/j.bone.2005.11.017 PubMedCrossRefGoogle Scholar
  68. 68.
    Spiegelman BM, Ginty CA (1983) Fibronectin modulation of cell shape and lipogenic gene expression in 3T3-adipocytes. Cell 35:657–666PubMedCrossRefGoogle Scholar
  69. 69.
    Kamiya S, Kato R, Wakabayashi M et al (2002) Fibronectin peptides derived from two distinct regions stimulate adipocyte differentiation by preventing fibronectin matrix assembly. Biochemistry 41:3270–3277. doi: 10.1021/bi015660a PubMedCrossRefGoogle Scholar
  70. 70.
    Luo W, Shitaye H, Friedman M et al (2008) Disruption of cell-matrix interactions by heparin enhances mesenchymal progenitor adipocyte differentiation. Exp Cell Res 314:3382–3391. doi: 10.1016/j.yexcr.2008.07.003 PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Noro A, Sillat T, Virtanen I et al (2013) Laminin production and basement membrane deposition by mesenchymal stem cells upon adipogenic differentiation. J Histochem Cytochem 61:719–730. doi: 10.1369/0022155413502055 PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Klein G (1995) The extracellular matrix of the hematopoietic microenvironment. Experientia 51:914–926. doi: 10.1007/BF01921741 PubMedCrossRefGoogle Scholar
  73. 73.
    Trotter TN, Yang Y (2016) Matricellular proteins as regulators of cancer metastasis to bone. Matrix Biol. doi: 10.1016/j.matbio.2016.01.006 PubMedGoogle Scholar
  74. 74.
    Oguri K, Okayama E, Caterson B, Okayama M (1987) Isolation, characterization, and localization of glycosaminoglycans in rabbit bone marrow. Blood 70:501–510PubMedGoogle Scholar
  75. 75.
    Delany AM, Hankenson KD (2009) Thrombospondin-2 and SPARC/osteonectin are critical regulators of bone remodeling. J Cell Commun Signal 3:227–238. doi: 10.1007/s12079-009-0076-0 PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Mansergh FC, Wells T, Elford C et al (2007) Osteopenia in Sparc (osteonectin)-deficient mice: characterization of phenotypic determinants of femoral strength and changes in gene expression. Physiol Genomics 32:64–73. doi: 10.1152/physiolgenomics.00151.2007 PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Shitaye HS, Terkhorn SP, Combs JA, Hankenson KD (2010) Thrombospondin-2 is an endogenous adipocyte inhibitor. Matrix Biol 29:549–556. doi: 10.1016/j.matbio.2010.05.006 PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Bi Y, Stuelten CH, Kilts T et al (2005) Extracellular matrix proteoglycans control the fate of bone marrow stromal cells. J Biol Chem 280:30481–30489. doi: 10.1074/jbc.M500573200 PubMedCrossRefGoogle Scholar
  79. 79.
    Nomiyama T, Perez-Tilve D, Ogawa D et al (2007) Osteopontin mediates obesity-induced adipose tissue macrophage infiltration and insulin resistance in mice. J Clin Invest 117:2877–2888. doi: 10.1172/JCI31986 PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Kong P, Gonzalez-Quesada C, Li N et al (2013) Thrombospondin-1 regulates adiposity and metabolic dysfunction in diet-induced obesity enhancing adipose inflammation and stimulating adipocyte proliferation. Am J Physiol Endocrinol Metab 305:E439–E450. doi: 10.1152/ajpendo.00006.2013 PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Wilsie LC, Chanchani S, Navaratna D, Orlando RA (2005) Cell surface heparan sulfate proteoglycans contribute to intracellular lipid accumulation in adipocytes. Lipids Health Dis 4:2. doi: 10.1186/1476-511X-4-2 PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Catalán V, Gómez-Ambrosi J, Rodríguez A, Frühbeck G (2012) Role of extracellular matrix remodelling in adipose tissue pathophysiology: relevance in the development of obesity. Histol Histopathol 27:1515–1528PubMedGoogle Scholar
  83. 83.
    Mariman EC, Wang P (2010) Adipocyte extracellular matrix composition, dynamics and role in obesity. Cell Mol Life Sci 67:1277–1292. doi: 10.1007/s00018-010-0263-4 PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Wang L, Mongera A, Bonanomi D et al (2014) A conserved axon type hierarchy governing peripheral nerve assembly. Development 141:1875–1883. doi: 10.1242/dev.106211 PubMedCrossRefGoogle Scholar
  85. 85.
    Holmgren S, Jensen J (2001) Evolution of vertebrate neuropeptides. Brain Res Bull 55:723–735PubMedCrossRefGoogle Scholar
  86. 86.
    Burnstock G (1969) Evolution of the autonomic innervation of visceral and cardiovascular systems in vertebrates. Pharmacol Rev 21:247–324PubMedGoogle Scholar
  87. 87.
    Sisask G, Bjurholm A, Ahmed M, Kreicbergs A (1995) Ontogeny of sensory nerves in the developing skeleton. Anat Rec 243:234–240. doi: 10.1002/ar.1092430210 PubMedCrossRefGoogle Scholar
  88. 88.
    Martini R, Schachner M (1991) Complex expression pattern of tenascin during innervation of the posterior limb buds of the developing chicken. J Neurosci Res 28:261–279. doi: 10.1002/jnr.490280214 PubMedCrossRefGoogle Scholar
  89. 89.
    Edoff K, Grenegård M, Hildebrand C (2000) Retrograde tracing and neuropeptide immunohistochemistry of sensory neurones projecting to the cartilaginous distal femoral epiphysis of young rats. Cell Tissue Res 299:193–200PubMedCrossRefGoogle Scholar
  90. 90.
    Dénes A, Boldogkoi Z, Uhereczky G et al (2005) Central autonomic control of the bone marrow: multisynaptic tract tracing by recombinant pseudorabies virus. Neuroscience 134:947–963. doi: 10.1016/j.neuroscience.2005.03.060 PubMedCrossRefGoogle Scholar
  91. 91.
    Bajayo A, Bar A, Denes A et al (2012) Skeletal parasympathetic innervation communicates central IL-1 signals regulating bone mass accrual. Proc Natl Acad Sci U S A 109:15455–15460. doi: 10.1073/pnas.1206061109 PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Mach DB, Rogers SD, Sabino MC et al (2002) Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroscience 113:155–166PubMedCrossRefGoogle Scholar
  93. 93.
    Yamazaki K, Allen TD (1990) Ultrastructural morphometric study of efferent nerve terminals on murine bone marrow stromal cells, and the recognition of a novel anatomical unit: the “neuro-reticular complex”. Am J Anat 187:261–276. doi: 10.1002/aja.1001870306 PubMedCrossRefGoogle Scholar
  94. 94.
    Duncan CP, Shim SS (1977) J. Edouard samson address: the autonomic nerve supply of bone. An experimental study of the intraosseous adrenergic nervi vasorum in the rabbit. J Bone Joint Surg Br 59:323–330PubMedGoogle Scholar
  95. 95.
    Elefteriou F, Ahn JD, Takeda S et al (2005) Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 434:514–520. doi: 10.1038/nature03398 PubMedCrossRefGoogle Scholar
  96. 96.
    Bartness TJ, Shrestha YB, Vaughan CH et al (2010) Sensory and sympathetic nervous system control of white adipose tissue lipolysis. Mol Cell Endocrinol 318:34–43. doi: 10.1016/j.mce.2009.08.031 PubMedCrossRefGoogle Scholar
  97. 97.
    Musso NR, Brenci S, Setti M et al (1996) Catecholamine content and in vitro catecholamine synthesis in peripheral human lymphocytes. J Clin Endocrinol Metab 81:3553–3557. doi: 10.1210/jcem.81.10.8855800 PubMedGoogle Scholar
  98. 98.
    Cosentino M, Marino F, Bombelli R et al (1999) Endogenous catecholamine synthesis, metabolism, storage and uptake in human neutrophils. Life Sci 64:975–981PubMedCrossRefGoogle Scholar
  99. 99.
    Marino F, Cosentino M, Bombelli R et al (1999) Endogenous catecholamine synthesis, metabolism storage, and uptake in human peripheral blood mononuclear cells. Exp Hematol 27:489–495PubMedCrossRefGoogle Scholar
  100. 100.
    Felten DL, Felten SY, Carlson SL et al (1985) Noradrenergic and peptidergic innervation of lymphoid tissue. J Immunol 135:755s–765sPubMedGoogle Scholar
  101. 101.
    Cosentino M, Marino F, Maestroni GJ (2015) Sympathoadrenergic modulation of hematopoiesis: a review of available evidence and of therapeutic perspectives. Front Cell Neurosci 9:302. doi: 10.3389/fncel.2015.00302 PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Katayama Y, Battista M, Kao WM et al (2006) Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124:407–421. doi: 10.1016/j.cell.2005.10.041 PubMedCrossRefGoogle Scholar
  103. 103.
    Arranz L, Sánchez-Aguilera A, Martín-Pérez D et al (2014) Neuropathy of haematopoietic stem cell niche is essential for myeloproliferative neoplasms. Nature 512:78–81. doi: 10.1038/nature13383 PubMedGoogle Scholar
  104. 104.
    Hanoun M, Zhang D, Mizoguchi T et al (2014) Acute myelogenous leukemia-induced sympathetic neuropathy promotes malignancy in an altered hematopoietic stem cell niche. Cell Stem Cell 15:365–375. doi: 10.1016/j.stem.2014.06.020 PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Hamrick MW, Della-Fera MA, Choi YH et al (2005) Leptin treatment induces loss of bone marrow adipocytes and increases bone formation in leptin-deficient ob/ob mice. J Bone Miner Res 20:994–1001. doi: 10.1359/JBMR.050103 PubMedCrossRefGoogle Scholar
  106. 106.
    Enriori PJ, Sinnayah P, Simonds SE et al (2011) Leptin action in the dorsomedial hypothalamus increases sympathetic tone to brown adipose tissue in spite of systemic leptin resistance. J Neurosci 31:12189–12197. doi: 10.1523/JNEUROSCI.2336-11.2011 PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Elefteriou F, Campbell P, Ma Y (2014) Control of bone remodeling by the peripheral sympathetic nervous system. Calcif Tissue Int 94:140–151. doi: 10.1007/s00223-013-9752-4 PubMedCrossRefGoogle Scholar
  108. 108.
    Mlakar V, Jurkovic Mlakar S, Zupan J et al (2015) ADRA2A is involved in neuro-endocrine regulation of bone resorption. J Cell Mol Med 19:1520–1529. doi: 10.1111/jcmm.12505 PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Kajimura D, Hinoi E, Ferron M et al (2011) Genetic determination of the cellular basis of the sympathetic regulation of bone mass accrual. J Exp Med 208:841–851. doi: 10.1084/jem.20102608 PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Pierroz DD, Bonnet N, Bianchi EN et al (2012) Deletion of β-adrenergic receptor 1, 2, or both leads to different bone phenotypes and response to mechanical stimulation. J Bone Miner Res 27:1252–1262. doi: 10.1002/jbmr.1594 PubMedCrossRefGoogle Scholar
  111. 111.
    Bouxsein ML, Devlin MJ, Glatt V et al (2009) Mice lacking beta-adrenergic receptors have increased bone mass but are not protected from deleterious skeletal effects of ovariectomy. Endocrinology 150:144–152. doi: 10.1210/en.2008-0843 PubMedCrossRefGoogle Scholar
  112. 112.
    Fonseca TL, Jorgetti V, Costa CC et al (2011) Double disruption of α2A- and α2C-adrenoceptors results in sympathetic hyperactivity and high-bone-mass phenotype. J Bone Miner Res 26:591–603. doi: 10.1002/jbmr.243 PubMedCrossRefGoogle Scholar
  113. 113.
    Takeda S, Elefteriou F, Levasseur R et al (2002) Leptin regulates bone formation via the sympathetic nervous system. Cell 111:305–317PubMedCrossRefGoogle Scholar
  114. 114.
    Hsiao EC, Boudignon BM, Chang WC et al (2008) Osteoblast expression of an engineered Gs-coupled receptor dramatically increases bone mass. Proc Natl Acad Sci U S A 105:1209–1214. doi: 10.1073/pnas.0707457105 PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Kinoshita T, Kobayashi S, Ebara S et al (2000) Phosphodiesterase inhibitors, pentoxifylline and rolipram, increase bone mass mainly by promoting bone formation in normal mice. Bone 27:811–817PubMedCrossRefGoogle Scholar
  116. 116.
    Wang L, Liu S, Quarles LD, Spurney RF (2005) Targeted overexpression of G protein-coupled receptor kinase-2 in osteoblasts promotes bone loss. Am J Physiol Endocrinol Metab 288:E826–E834. doi: 10.1152/ajpendo.00422.2004 PubMedCrossRefGoogle Scholar
  117. 117.
    Imai S, Tokunaga Y, Maeda T et al (1997) Calcitonin gene-related peptide, substance P, and tyrosine hydroxylase-immunoreactive innervation of rat bone marrows: an immunohistochemical and ultrastructural investigation on possible efferent and afferent mechanisms. J Orthop Res 15:133–140. doi: 10.1002/jor.1100150120 PubMedCrossRefGoogle Scholar
  118. 118.
    Loaiza LA, Yamaguchi S, Ito M, Ohshima N (2002) Vasodilatation of muscle microvessels induced by somatic afferent stimulation is mediated by calcitonin gene-related peptide release in the rat. Neurosci Lett 333:136–140PubMedCrossRefGoogle Scholar
  119. 119.
    Supowit SC, Ethridge RT, Zhao H et al (2005) Calcitonin gene-related peptide and substance P contribute to reduced blood pressure in sympathectomized rats. Am J Physiol Heart Circ Physiol 289:H1169–H1175. doi: 10.1152/ajpheart.00973.2004 PubMedCrossRefGoogle Scholar
  120. 120.
    Norevall LI, Matsson L, Forsgren S (1998) Main sensory neuropeptides, but not VIP and NPY, are involved in bone remodeling during orthodontic tooth movement in the rat. Ann N Y Acad Sci 865:353–359PubMedCrossRefGoogle Scholar
  121. 121.
    Imai S, Matsusue Y (2002) Neuronal regulation of bone metabolism and anabolism: calcitonin gene-related peptide-, substance P-, and tyrosine hydroxylase-containing nerves and the bone. Microsc Res Tech 58:61–69. doi: 10.1002/jemt.10119 PubMedCrossRefGoogle Scholar
  122. 122.
    Miegueu P, St-Pierre DH, Lapointe M et al (2013) Substance P decreases fat storage and increases adipocytokine production in 3T3-L1 adipocytes. Am J Physiol Gastrointest Liver Physiol 304:G420–G427. doi: 10.1152/ajpgi.00162.2012 PubMedCrossRefGoogle Scholar
  123. 123.
    Chatzipanteli K, Goldbergt RB, Howard G, Roos BA (1996) Calcitonin gene-related peptide is an adipose-tissue neuropeptide with lipolytic actions. Endocrinol Metab 3:235–242Google Scholar
  124. 124.
    Lundberg P, Lerner UH (2002) Expression and regulatory role of receptors for vasoactive intestinal peptide in bone cells. Microsc Res Tech 58:98–103. doi: 10.1002/jemt.10124 PubMedCrossRefGoogle Scholar
  125. 125.
    Schinke T, Liese S, Priemel M et al (2004) Decreased bone formation and osteopenia in mice lacking alpha-calcitonin gene-related peptide. J Bone Miner Res 19:2049–2056. doi: 10.1359/JBMR.040915 PubMedCrossRefGoogle Scholar
  126. 126.
    Danaher RN, Loomes KM, Leonard BL et al (2008) Evidence that alpha-calcitonin gene-related peptide is a neurohormone that controls systemic lipid availability and utilization. Endocrinology 149:154–160. doi: 10.1210/en.2007-0583 PubMedCrossRefGoogle Scholar
  127. 127.
    Conlon JM, O’Harte F, Peter RE, Kah O (1991) Carassin: a tachykinin that is structurally related to neuropeptide-gamma from the brain of the goldfish. J Neurochem 56:1432–1436PubMedCrossRefGoogle Scholar
  128. 128.
    Rameshwar P, Ganea D, Gascón P (1993) In vitro stimulatory effect of substance P on hematopoiesis. Blood 81:391–398PubMedGoogle Scholar
  129. 129.
    Imai S, Rauvala H, Konttinen YT et al (1997) Efferent targets of osseous CGRP-immunoreactive nerve fiber before and after bone destruction in adjuvant arthritic rat: an ultramorphological study on their terminal-target relations. J Bone Miner Res 12:1018–1027. doi: 10.1359/jbmr.1997.12.7.1018 PubMedCrossRefGoogle Scholar
  130. 130.
    Guo TZ, Wei T, Shi X et al (2012) Neuropeptide deficient mice have attenuated nociceptive, vascular, and inflammatory changes in a tibia fracture model of complex regional pain syndrome. Mol Pain 8:85. doi: 10.1186/1744-8069-8-85 PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Cherruau M, Facchinetti P, Baroukh B, Saffar JL (1999) Chemical sympathectomy impairs bone resorption in rats: a role for the sympathetic system on bone metabolism. Bone 25:545–551PubMedCrossRefGoogle Scholar
  132. 132.
    Niijima A (1999) Reflex effects from leptin sensors in the white adipose tissue of the epididymis to the efferent activity of the sympathetic and vagus nerve in the rat. Neurosci Lett 262:125–128PubMedCrossRefGoogle Scholar
  133. 133.
    Niijima A (1998) Afferent signals from leptin sensors in the white adipose tissue of the epididymis, and their reflex effect in the rat. J Auton Nerv Syst 73:19–25PubMedCrossRefGoogle Scholar
  134. 134.
    Camus A, Berliner A, Clauss T et al (2013) Serratia marcescens associated ampullary system infection and septicaemia in a bonnethead shark, sphyrna tiburo (L.). J Fish Dis 36:891–895. doi: 10.1111/jfd.12107 PubMedCrossRefGoogle Scholar
  135. 135.
    Kent ML, Spitsbergen JM, Matthews JM, et al. (2012) ZIRC Health Services Zebrafish Disease Manual. In: Diseases of Zebrafish in Research Facilities. http://zebrafish.org/health/diseaseManual.php. Accessed 16 May 2016

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Cell Biology & PhysiologyWashington UniversitySaint LouisUSA
  2. 2.Division of Bone and Mineral Diseases, Department of Internal MedicineWashington UniversitySaint LouisUSA

Personalised recommendations