The NPY system and its neural and neuroendocrine regulation of bone

Current Osteoporosis Reports

Volumn 10, Issue 2, 2012, Pages 160-168

  Khor, Ee Cheng ^a   Baldock, Paul ^a  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Bone remodeling; Hypothalamus; Mouse model; Neuropeptide Y; NPY; Osteoblast; Peptide YY; Sympathetic nervous system

Indexed keywords

NEUROPEPTIDE Y; NEUROPEPTIDE Y RECEPTOR; NEUROPEPTIDE Y1 RECEPTOR; NEUROPEPTIDE Y2 RECEPTOR; NEUROPEPTIDE Y4; NEUROPEPTIDE Y5 RECEPTOR; NEUROPEPTIDE Y6 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BONE CELL; BONE MASS; BONE METABOLISM; CELL ACTIVITY; HIP FRACTURE; HOMEOSTASIS; HUMAN; HYPOTHALAMUS; MORBIDITY; MORTALITY; NEUROENDOCRINE SYSTEM; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOPOROSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BONE AND BONES; HOMEOSTASIS; HUMANS; MICE; MODELS, ANIMAL; NEURAL PATHWAYS; NEUROPEPTIDE Y; NEUROSECRETORY SYSTEMS; SIGNAL TRANSDUCTION;

EID: 84865785443     PISSN: 15441873     EISSN: 15442241     Source Type: Journal    
DOI: 10.1007/s11914-012-0102-7     Document Type: Article

References (85)

1. Baron R. Anatomy and ultrastructure of bone. In: Favus MF, editor. Primer on the metabolic bone diseases and disorders of mineral metabolism. 4th ed. Philadelphia PA: Lippincott Williams and Wilkins; 1999. p. 3-10.
2. Sambrook P, Cooper C. Osteoporosis. Lancet. 2006;367 (9527):2010-8. (Pubitemid 43867702)
3. Gordeladze JO, Reseland JE. A unified model for the action of leptin on bone turnover. Journal of cellular biochemistry. 2003;88 (4):706-12. (Pubitemid 36258820)
4. Tatemoto K, Carlquist M, Mutt V. Neuropeptide Y - a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature. 1982;296(5858):659-60. (Pubitemid 12089070)
5. Baraban SC. Neuropeptide Y and limbic seizures. Reviews in the Neurosciences. 1998;9(2):117-28. (Pubitemid 28386643)
6. Lin S, Boey D, Herzog H. NPY and Y receptors: lessons from transgenic and knockout models. Neuropeptides. 2004;38:189-200. (Pubitemid 39161911)
7. Ekblad E, Edvinsson L, Wahlestedt C, et al. Neuropeptide Y coexists and co-operates with noradrenaline in perivascular nerve fibers. Regul Pept. 1984;8(3):225-35. (Pubitemid 14109276)
8. Baldock PA, Allison SJ, Lundberg P, et al. Novel role of Y1 receptors in the coordinated regulation of bone and energy homeostasis. J Biol Chem. 2007;282(26):19092-102. (Pubitemid 47100174)
9. Kuo LE, Kitlinska JB, Tilan JU, et al. Neuropeptide Y acts directly in the periphery on fat tissue and mediates stress-induced obesity and metabolic syndrome. Nat Med. 2007;13(7):803-11. (Pubitemid 47038195)
10. Yang K, Guan H, Arany E, et al. Neuropeptide Y is produced in visceral adipose tissue and promotes proliferation of adipocyte precursor cells via the Y1 receptor. Faseb J. 2008;22 (7):2452-64. (Pubitemid 351948663)
11. Schwartz TW, Fuhlendorff J, Kjems LL, et al. Signal Epitopes in the Three-Dimensional Structure of Neuropeptide Y Annals of the New York Academy of Sciences. 1990;611(1):35-47.
12. Nordmann A, Blommers MJJ, Fretz H, et al. Aspects of the molecular structure and dynamics of neuropeptide Y European Journal of Biochemistry. 1999;261(1):216-26. (Pubitemid 29166087)
13. Blomqvist AG, Herzog H. Y-receptor subtypes-how many more? Trends Neurosci. 1997;20(7):294-8.
14. Michel MC, Beck-Sickinger A, Cox H, et al. XVI. International union of pharmacology recommendations for the nomenclature of neuropeptide Y, peptide YY, and pancreatic polypeptide receptors. Pharmacol Rev. 1998;50(1):143-50. (Pubitemid 28158845)
15. Parker RM, Herzog H. Regional distribution of Y-receptor subtype mRNAs in rat brain. Eur J Neurosci. 1999;11(4):1431-48. (Pubitemid 29142202)
16. Naveilhan P, Neveu I, Arenas E, Ernfors P. Complementary and overlapping expression of Y1, Y2 and Y5 receptors in the developing and adult mouse nervous system. Neuroscience. 1998;87 (1):289-302. (Pubitemid 28351185)
17. Gerald C, Walker MW, Criscione L, et al.: A receptor subtype involved in neuropeptide-Y-induced food intake. Nature [10.1038/382168a0]. 1996, 382(6587):168-71. (Pubitemid 26242883)
18. Gregor P, Feng Y, DeCarr LB, et al. Molecular characterization of a second mouse pancreatic polypeptide receptor and its inactivated human homologue. J Biol Chem. 1996;271(44):27776-81. (Pubitemid 26367351)
19. Weinberg DH, Sirinathsinghji DJ, Tan CP, et al. Cloning and expression of a novel neuropeptide Y receptor. J Biol Chem. 1996;271(28):16435-8. (Pubitemid 26238989)
20. Lee NJ, Doyle KL, Sainsbury A, et al: Critical role for Y1 receptors in mesenchymal progenitor cell differentiation and osteoblast activity. J Bone Miner Res 2010, 25(8):1736-47.
21. Lundberg P, Allison SJ, Lee NJ, et al Greater bone formation of Y2 knockout mice is associated with increased osteoprogenitor numbers and altered Y1 receptor expression. J Biol Chem. 2007;282(26):19082-91. (Pubitemid 47100173)
22. Gerald C, Walker MW, Vaysse PJ, et al Expression cloning and pharmacological characterization of a human hippocampal neuropeptide Y/peptide YY Y2 receptor subtype. The Journal of biological chemistry. 1995;270(45):26758-61.
23. Herzog H, Hort YJ, Ball HJ, et al. Cloned human neuropeptide Y receptor couples to two different second messenger systems. Proc Natl Acad Sci U S A. 1992;89(13):5794-8.
24. Motulsky HJ, Michel MC. Neuropeptide Y mobilizes Ca2+ and inhibits adenylate cyclase in human erythroleukemia cells. Am J Physiol. 1988;255(6 Pt 1):E880-5.
25. Xiong Z, Cheung DW. ATP-Dependent inhibition of Ca2+-activated K+ channels in vascular smooth muscle cells by neuropeptide Y. Pflugers Arch. 1995;431(1):110-6.
26. Nakamura M, Sakanaka C, Aoki Y, et al. Identification of two isoforms of mouse neuropeptide Y-Y1 receptor generated by alternative splicing. Isolation, genomic structure, and functional expression of the receptors. The Journal of biological chemistry. 1995;270(50):30102-10.
27. Nie M, Selbie LA. Neuropeptide Y Y1 and Y2 receptor-mediated stimulation of mitogen-activated protein kinase activity. Regul Pept. 1998;75-76:207-13. (Pubitemid 28477529)
28. Ruscica M, Dozio E, Boghossian S, et al. Activation of the Y1 receptor by neuropeptide Y regulates the growth of prostate cancer cells. Endocrinology. 2006;147(3):1466-73. (Pubitemid 43244381)
29. Keffel S, Schmidt M, Bischoff A, Michel MC. Neuropeptide-Y stimulation of extracellular signal-regulated kinases in human erythroleukemia cells. J Pharmacol Exp Ther. 1999;291 (3):1172-8.
30. Cho YR, Kim CW. Neuropeptide Y promotes beta-cell replication via extracellular signal-regulated kinase activation. Biochemical and biophysical research communications. 2004;314(3):773-80. (Pubitemid 38112865)
31. Mannon PJ, Mele JM. Peptide YY Y1 receptor activates mitogen-activated protein kinase and proliferation in gut epithelial cells via the epidermal growth factor receptor. Biochem J. 2000;350(Pt 3):655-61.
32. Hill EL, Elde R. Distribution of CGRP-, VIP-, D beta H-, SP-, and NPY-immunoreactive nerves in the periosteum of the rat. Cell Tissue Res. 1991;264(3):469-80.
33. Ahmed M, Bjurholm A, Kreicbergs A, Schultzberg M. Neuropeptide Y, tyrosine hydroxylase and vasoactive intestinal polypeptide-immunoreactive nerve fibers in the vertebral bodies, discs, dura mater, and spinal ligaments of the rat lumbar spine. Spine. 1993;18(2):268-73. (Pubitemid 23063166)
34. Bjurholm A, Kreicbergs A, Terenius L, et al. Neuropeptide Y-, tyrosine hydroxylase- and vasoactive intestinal polypeptide-immunoreactive nerves in bone and surrounding tissues. Journal of the autonomic nervous system. 1988;25(2-3):119-25. (Pubitemid 19057144)
35. Malmstrom RE. Vascular pharmacology of BIIE0246, the first selective non-peptide neuropeptide Y Y(2) receptor antagonist, in vivo. Br J Pharmacol. 2001;133(7):1073-80. (Pubitemid 32762418)
36. Sisask G, Bjurholm A, Ahmed M, Kreicbergs A. The development of autonomic innervation in bone and joints of the rat. J Auton Nerv Syst. 1996;59(1-2):27-33. (Pubitemid 26227671)
37. Mercer JG, Hoggard N, Williams LM, et al. Coexpression of leptin receptor and preproneuropeptide Y mRNA in arcuate nucleus of mouse hypothalamus. J Neuroendocrinol. 1996;8(10):733-5. (Pubitemid 26331795)
38. Erickson JC, Hollopeter G, Palmiter RD. Attenuation of the obesity syndrome of ob/ob mice by the loss of neuropeptide Y. Science. 1996;274(5293):1704-7. (Pubitemid 26414900)
39. Ducy P, Amling M, Takeda S, et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell. 2000;100(2):197-207. (Pubitemid 30064908)
40. Iwaniec UT, Boghossian S, Lapke PD, et al. Central leptin gene therapy corrects skeletal abnormalities in leptin-deficient ob/ob mice. Peptides. 2007;28(5):1012-9. (Pubitemid 46654437)
41. Takeda S, Elefteriou F, Levasseur R, et al. Leptin Regulates Bone Formation via the Sympathetic Nervous System. Cell. 2002;111 (3):305-17. (Pubitemid 35345151)
42. Baldock PA, Allison S, McDonald MM, et al. Hypothalamic regulation of cortical bone mass: opposing activity of Y2 receptor and leptin pathways. J Bone Miner Res. 2006;21 (10):1600-7. (Pubitemid 44484605)
43. Baldock PA, Sainsbury A, Allison S, et al. Hypothalamic control of bone formation: distinct actions of leptin and y2 receptor pathways. J Bone Miner Res. 2005;20(10):1851-7. (Pubitemid 41361887)
44. Allison S, Baldock P, Enriquez R, et al.: Critical Interplay Between Neuropeptide Y and Sex Steroid Pathways in Bone and Adipose Tissue Homeostasis. J Bone Miner Res. 2008 Oct 10.
45. Baldock PA, Lee NJ, Driessler F, et al.: Neuropeptide Y knockout mice reveal a central role of NPY in the coordination of bone mass to body weight. PLoS One. 2009, 4(12):e8415.
46. Elefteriou F, Takeda S, Liu X, et al. Monosodium glutamatesensitive hypothalamic neurons contribute to the control of bone mass. Endocrinology. 2003;144(9):3842-7. (Pubitemid 37088737)
47. Fetissov SO, Byrne LC, Hassani H, et al. Characterization of neuropeptide Y Y2 and Y5 receptor expression in the mouse hypothalamus. J Comp Neurol. 2004;470(3):256-65. (Pubitemid 38160680)
48. Lin S, Boey D, Couzens M, et al. Compensatory changes in [125I]-PYY binding in Y receptor knockout mice suggest the potential existence of further Y receptor(s). Neuropeptides. 2005;39(1):21-8. (Pubitemid 41373325)
49. Broberger C, Landry M, Wong H, et al. Subtypes Y1 and Y2 of the neuropeptide Y receptor are respectively expressed in proopiomelanocortin- and neuropeptide-Y-containing neurons of the rat hypothalamic arcuate nucleus. Neuroendocrinology. 1997;66 (6):393-408. (Pubitemid 27500899)
50. King PJ, Williams G, Doods H, Widdowson PS. Effect of a selective neuropeptide Y Y(2) receptor antagonist, BIIE0246 on neuropeptide Y release. Eur J Pharmacol. 2000;396(1):R1-3. (Pubitemid 30261560)
51. Baldock PA, Sainsbury A, Couzens M, et al. Hypothalamic Y2 receptors regulate bone formation. J Clin Invest. 2002;109(7):915-21. (Pubitemid 34275112)
52. Allison SJ, Baldock P, Sainsbury A, et al. Conditional deletion of hypothalamic Y2 receptors reverts gonadectomy-induced bone loss in adult mice. J Biol Chem. 2006;281(33):23436-44. (Pubitemid 44274118)
53. Shi YC, Lin S, Wong IP, et al.: NPY neuron-specific Y2 receptors regulate adipose tissue and trabecular bone but not cortical bone homeostasis in mice. PLoS One. 2010, 5(6):e11361.
54. Dumont Y, Fournier A, St-Pierre S, et al. Differential distribution of neuropeptide Y1 and Y2 receptors in the rat brain. European Journal of Pharmacology. 1990;191(3):501-3.
55. Bjurholm A. Neuroendocrine peptides in bone. Int Orthop. 1991;15(4):325-9.
56. Bjurholm A, Kreicbergs A, Schultzberg M, Lerner UH. Neuroendocrine regulation of cyclic AMP formation in osteoblastic cell lines (UMR-106-01, ROS 17/2.8, MC3T3-E1, and Saos-2) and primary bone cells. J Bone Miner Res. 1992;7(9):1011-9.
57. Igwe JC, Jiang X, Paic F, et al.: Neuropeptide Y is expressed by osteocytes and can inhibit osteoblastic activity. J Cell Biochem. 2009 Oct 15, 108(3):621-30.
58. Amano S, Arai M, Goto S, Togari A. Inhibitory effect of NPY on isoprenaline-induced osteoclastogenesis in mouse bone marrow cells. Biochim Biophys Acta. 2007;1770(6):966-73. (Pubitemid 46617038)
59. Lundberg JM, Martinsson A, Hemsen A, et al. Co-release of neuropeptide Y and catecholamines during physical exercise in man. Biochemical and Biophysical Research Communications. 1985;133(1):30-6. (Pubitemid 16155324)
60. Kempna P, Korner M, Waser B, et al. Neuropeptide Y modulates steroid production of human adrenal H295R cells through Y1 receptors. Mol Cell Endocrinol. 2010;314(1):101-9.
61. Morgan DG, Kulkarni RN, Hurley JD, et al. Inhibition of glucose stimulated insulin secretion by neuropeptide Y is mediated via the Y1 receptor and inhibition of adenylyl cyclase in RIN 5AH rat insulinoma cells. Diabetologia. 1998;41(12):1482-91. (Pubitemid 28551620)
62. Ishizuka K, Hirukawa K, Nakamura H, Togari A. Inhibitory effect of CGRP on osteoclast formation by mouse bone marrow cells treated with isoproterenol. Neurosci Lett. 2005;379(1):47-51. (Pubitemid 40462396)
63. Teixeira L, Sousa DM, Nunes AF, et al.: NPY revealed as a critical modulator of osteoblast function in vitro: New insights into the role of Y1 and Y2 receptors. J Cell Biochem. 2009 May 20.
64. Goumain M, Voisin T, Lorinet AM, Laburthe M. Identification and distribution of mRNA encoding the Y1, Y2, Y4, and Y5 receptors for peptides of the PP-fold family in the rat intestine and colon. Biochem Biophys Res Commun. 1998;247(1):52-6. (Pubitemid 28412523)
65. Wharton J, Gordon L, Byrne J, et al. Expression of the human neuropeptide tyrosine Y1 receptor. Proc Natl Acad Sci U S A. 1993;90(2):687-91. (Pubitemid 23028929)
66. Lee NJ, Nguyen AD, Enriquez RF, et al. Osteoblast specific Y1 receptor deletion enhances bone mass. Bone. 2011;48(3):461-7.
67. Playford RJ, Cox HM. Peptide YY and neuropeptide Y: two peptides intimately involved in electrolyte homeostasis. Trends in Pharmacological Scineces. 1996;17(12):436-8. (Pubitemid 27028473)
68. Shi YC, Lin S, Castillo L, et al.: Peripheral-Specific Y2 Receptor Knockdown Protects Mice From High-Fat Diet-Induced Obesity. Obesity (Silver Spring). 2011 May 5.
69. Koda S, Date Y, Murakami N, et al. The role of the vagal nerve in peripheral PYY3-36-induced feeding reduction in rats. Endocrinology. 2005;23:305-21.
70. Sainsbury A, Baldock PA, Schwarzer C, et al. Synergistic effects of Y2 and Y4 receptors on adiposity and bone mass revealed in double knockout mice. Mol Cell Biol. 2003;23(15):5225-33. (Pubitemid 36950878)
71. Wortley KE, Garcia K, Okamoto H, et al. Peptide YY regulates bone turnover in rodents. Gastroenterology. 2007;133(5):1534-43. (Pubitemid 350029744)
72. Cornish J, Callon KE, King AR, et al. Systemic administration of amylin increases bone mass, linear growth, and adiposity in adult male mice. Am J Physiol. 1998;275(4 Pt 1):E694-9.
73. Henriksen DB, Alexandersen P, Bjarnason NH, et al. Role of gastrointestinal hormones in postprandial reduction of bone resorption. J Bone Miner Res. 2003;18(12):2180-9. (Pubitemid 37463311)
74. van der Velde M, Delhanty P, van der Eerden B, et al. Ghrelin and bone. Vitam Horm. 2008;77:239-58.
75. Misra M, Miller KK, Tsai P, et al. Elevated peptide YY levels in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab. 2006;91(3):1027-33. (Pubitemid 43357776)
76. Utz AL, Lawson EA, Misra M, et al. Peptide YY (PYY) levels and bone mineral density (BMD) in women with anorexia nervosa. Bone. 2008;43(1):135-9.
77. Scheid JL, Toombs RJ, Ducher G, et al. Estrogen and peptide YY are associated with bone mineral density in premenopausal exercising women. Bone. 2011;49(2):194-201 [Research Support, U. S. Gov't, Non-P.H.S.].
78. Herzog H, Darby K, Ball H, et al. Overlapping gene structure of the human neuropeptide Y receptor subtypes Y1 and Y5 suggests coordinate transcriptional regulation. Genomics. 1997;41(3):315-9. (Pubitemid 27194781)
79. Igura K, Haider H, Ahmed RP, et al. Neuropeptide y and neuropeptide y y5 receptor interaction restores impaired growth potential of aging bone marrow stromal cells. Rejuvenation Res. 2011;14 (4):393-403.
80. Reid IR. Relationships between fat and bone. Osteoporos Int. 2008;19(5):595-606. (Pubitemid 351642171)
81. Reid IR, Plank LD, Evans MC. Fat mass is an important determinant of whole body bone density in premenopausal women but not in men. J Clin Endocrinol Metab. 1992;75(3):779-82.
82. Nguyen ND, Pongchaiyakul C, Center JR, et al. Identification of high-risk individuals for hip fracture: a 14-year prospective study. J Bone Miner Res. 2005;20(11):1921-8. Epub 2005 May 31. (Pubitemid 41532777)
83. Nguyen ND, Pongchaiyakul C, Center JR, et al. Abdominal fat and hip fracture risk in the elderly: the Dubbo Osteoporosis Epidemiology Study. BMC Musculoskelet Disord. 2005;6:11.
84. De Laet C, Kanis JA, Oden A, et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int. 2005;16(11):1330-8. (Pubitemid 41532085)
85. Nguyen TV, Sambrook PN, Eisman JA. Bone loss, physical activity, and weight change in elderly women: the Dubbo Osteoporosis Epidemiology Study. J Bone Miner Res. 1998;13(9):1458-67. (Pubitemid 28418913)