Skeletal parasympathetic innervation communicates central IL-1 signals regulating bone mass accrual

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 38, 2012, Pages 15455-15460

  Bajayo, Alon ^a   Bar, Arik ^a   Denes, Adam ^b,c   Bachar, Marilyn ^a   Kram, Vardit ^a   Attar Namdar, Malka ^a   Zallone, Alberta ^d   Kovács, Krisztina J ^c   Yirmiya, Raz ^a   Bab, Itai ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d UNIVERSITY OF BARI   (Italy)

Author keywords

Autonomic nervous system; Postnatal skeletal development

Indexed keywords

CHOLINERGIC RECEPTOR; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; NICOTINIC RECEPTOR; PYRIDOSTIGMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE CELL; BONE MASS; BONE REMODELING; CELL PROLIFERATION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE SILENCING; MALE; MORPHOMETRICS; MOUSE; NERVE FIBER; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PARASYMPATHETIC INNERVATION; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPINAL CORD; SYMPATHETIC TONE;

ACETYLCHOLINE; ANIMALS; APOPTOSIS; BONE AND BONES; BONE DENSITY; BONE RESORPTION; BRAIN; CELL PROLIFERATION; HEART; HUMANS; INTERLEUKIN-1; MALE; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; OSTEOBLASTS; OSTEOCLASTS; PARASYMPATHETIC NERVOUS SYSTEM; PYRIDOSTIGMINE BROMIDE; SIGNAL TRANSDUCTION;

MUS; SUID HERPESVIRUS 1;

EID: 84866542685     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1206061109     Document Type: Article

References (50)

1. Rodan GA, Martin TJ (2000) Therapeutic approaches to bone diseases. Science 289: 1508-1514.
2. Elefteriou F, et al. (2005) Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 434:514-520. (Pubitemid 40477060)
3. Katayama Y, et al. (2006) Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124:407-421. (Pubitemid 43121987)
4. Yirmiya R, et al. (2006) Depression induces bone loss through stimulation of the sympathetic nervous system. Proc Natl Acad Sci USA 103:16876-16881. (Pubitemid 44737346)
5. Tam J, et al. (2008) The cannabinoid CB1 receptor regulates bone formation by modulating adrenergic signaling. FASEB J 22:285-294.
6. Johnson RH, Spaulding JM (1974) Disorders of the autonomic nervous system. Chapter 3. The nervous control of the circulation and its investigation. Contemp Neurol Ser 11: 33-58.
7. Kawasaki A (1999) Physiology, assessment, and disorders of the pupil. Curr Opin Ophthalmol 10:394-400.
8. Kiba T (2004) Relationships between the autonomic nervous system and the pancreas including regulation of regeneration and apoptosis: Recent developments. Pancreas 29:e51-e58.
9. Manabe N, Tanaka T, Hata J, Kusunoki H, Haruma K (2009) Pathophysiology underlying irritable bowel syndrome-From the viewpoint of dysfunction of autonomic nervous system activity. J Smooth Muscle Res 45:15-23.
10. Young JA, Van Lennep EW (1977) Morphology and physiology of salivary myoepithelial cells. Int Rev Physiol 12:105-125.
11. Kandel ER, Schwartz JH, Jessell TM (2000) Principles of Neural Science (McGraw-Hill, New York), 4th Ed.
12. Loewi O (1921) Über humorale Übertragbarkeit der Herznervenwirkung [About humoral transmission of cardiac nerves effect]. Pflugers Arch, 189:239-242. German.
13. Nachmansohn D, John HM (1945) On the formation of acetylcholine in the nerve axon. Science 102:250-251.
14. Schäfer MK, Weihe E, Varoqui H, Eiden LE, Erickson JD (1994) Distribution of the vesicular acetylcholine transporter (VAChT) in the central and peripheral nervous systems of the rat. J Mol Neurosci 5:1-26.
15. Weihe E, Tao-Cheng JH, Schäfer MK, Erickson JD, Eiden LE (1996) Visualization of the vesicular acetylcholine transporter in cholinergic nerve terminals and its targeting to a specific population of small synaptic vesicles. Proc Natl Acad Sci USA 93:3547-3552. (Pubitemid 26125658)
16. Dani JA, Bertrand D (2007) Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol 47:699-729.
17. Caulfield MP, Birdsall NJ (1998) International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50:279-290. (Pubitemid 28304029)
18. Taylor P, Radić Z (1994) The cholinesterases: From genes to proteins. Annu Rev Pharmacol Toxicol 34:281-320.
19. Shi Y, et al. (2010) Signaling through the M(3) muscarinic receptor favors bone mass accrual by decreasing sympathetic activity. Cell Metab 11:231-238.
20. En-Nosse M, et al. (2009) Expression of non-neuronal cholinergic system in osteoblast-like cells and its involvement in osteogenesis. Cell Tissue Res 338:203-215.
21. Krueger JM, et al. (1998) Sleep. A physiologic role for IL-1 beta and TNF-alpha. Ann N Y Acad Sci 856:148-159. (Pubitemid 128713055)
22. Avital A, et al. (2003) Impaired interleukin-1 signaling is associated with deficits in hippocampal memory processes and neural plasticity. Hippocampus 13:826-834. (Pubitemid 37407969)
23. Bajayo A, et al. (2005) Central IL-1 receptor signaling regulates bone growth and mass. Proc Natl Acad Sci USA 102:12956-12961. (Pubitemid 41279471)
24. Dénes A, et al. (2005) Central autonomic control of the bone marrow: Multisynaptic tract tracing by recombinant pseudorabies virus. Neuroscience 134:947-963. (Pubitemid 41133397)
25. Trotter RN, Stornetta RL, Guyenet PG, Roberts MR (2007) Transneuronal mapping of the CNS network controlling sympathetic outflow to the rat thymus. Auton Neurosci 131:9-20. (Pubitemid 44960170)
26. Cano G, Sved AF, Rinaman L, Rabin BS, Card JP (2001) Characterization of the central nervous system innervation of the rat spleen using viral transneuronal tracing. J Comp Neurol 439:1-18.
27. Tien D, Ohara PT, Larson AA, Jasmin L (2003) Vagal afferents are necessary for the establishment but not the maintenance of kainic acid-induced hyperalgesia in mice. Pain 102:39-49. (Pubitemid 36298860)
28. Marritt AM, et al. (2005) Nicotinic cholinergic receptors in the rat retina: Simple and mixed heteromeric subtypes. Mol Pharmacol 68:1656-1668. (Pubitemid 41654349)
29. Whiteaker P, et al. (2009) Pharmacological and immunochemical characterization of alpha2*nicotinic acetylcholine receptors (nAChRs) in mouse brain. Acta Pharmacol Sin 30:795-804.
30. Martin BR, Onaivi ES, Martin TJ (1989) What is the nature of mecamylamine's antagonism of the central effects of nicotine? Biochem Pharmacol 38:3391-3397. (Pubitemid 19250188)
31. Suda T, Jimi E, Nakamura I, Takahashi N (1997) Role of 1 alpha,25-dihydroxyvitamin D3 in osteoclast differentiation and function. Methods Enzymol 282:223-235. (Pubitemid 27412778)
32. Rothem DE, Rothem L, Soudry M, Dahan A, Eliakim R (2009) Nicotine modulates bone metabolism-associated gene expression in osteoblast cells. J Bone Miner Metab 27: 555-561.
33. Pedersen SE, Cohen JB (1990) d-Tubocurarine binding sites are located at alpha-gamma and alpha-delta subunit interfaces of the nicotinic acetylcholine receptor. Proc Natl Acad Sci USA 87:2785-2789.
34. Masson P (2011) Evolution of and perspectives on therapeutic approaches to nerve agent poisoning. Toxicol Lett 206:5-13.
35. Buisson B, Bertrand D (2002) Nicotine addiction: The possible role of functional upregulation. Trends Pharmacol Sci 23:130-136. (Pubitemid 34185414)
36. Qin W, Bauman WA, Cardozo CP (2010) Evolving concepts in neurogenic osteoporosis. Curr Osteoporos Rep 8:212-218.
37. Romano SJ, Pugh PC, McIntosh JM, Berg DK (1997) Neuronal-type acetylcholine receptors and regulation of alpha 7 gene expression in vertebrate skeletal muscle. J Neurobiol 32:69-80. (Pubitemid 27020246)
38. Maletic V, Raison CL (2009) Neurobiology of depression, fibromyalgia and neuropathic pain. Front Biosci 14:5291-5338.
39. Liu PS, Chen YY, Feng CK, Lin YH, Yu TC (2011) Muscarinic acetylcholine receptors present in human osteoblast and bone tissue. Eur J Pharmacol 650:34-40.
40. Proskocil BJ, et al. (2004) Acetylcholine is an autocrine or paracrine hormone synthesized and secreted by airway bronchial epithelial cells. Endocrinology 145: 2498-2506. (Pubitemid 38535077)
41. Sato T, et al. (2010) Functional role of acetylcholine and the expression of cholinergic receptors and components in osteoblasts. FEBS Lett 584:817-824.
42. Yirmiya R, Bab I (2009) Major depression is a risk factor for low bone mineral density: A meta-analysis. Biol Psychiatry 66:423-432.
43. Pack AM, Reddy DS, Duncan S, Herzog A (2011) Neuroendocrinological aspects of epilepsy: Important issues and trends in future research. Epilepsy Behav 22:94-102.
44. Mineur YS, Picciotto MR (2010) Nicotine receptors and depression: Revisiting and revising the cholinergic hypothesis. Trends Pharmacol Sci 31:580-586.
45. Miwa JM, Freedman R, Lester HA (2011) Neural systems governed by nicotinic acetylcholine receptors: Emerging hypotheses. Neuron 70:20-33.
46. Sullivan GM, et al. (1997) Intracerebroventricular injection of interleukin-1 suppresses peripheral lymphocyte function in the primate. Neuroimmunomodulation 4:12-18. (Pubitemid 27397854)
47. Rosas-Ballina M, et al. (2008) Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. Proc Natl Acad Sci USA 105: 11008-11013.
48. Colucci S, Colaianni G, Mori G, Grano M, Zallone A (2002) Human osteoclasts express oxytocin receptor. Biochem Biophys Res Commun 297:442-445.
49. Brown OM (1976) Cat heart acetylcholine: Structural proof and distribution. Am J Physiol 231:781-785.
50. Smoum R, et al. (2010) Oleoyl serine, an endogenous N-acyl amide, modulates bone remodeling and mass. Proc Natl Acad Sci USA 107:17710-17715.