Osteocalcin is a stress-responsive neuropeptide

Endocrine Regulations

Volumn 45, Issue 2, 2011, Pages 99-110

  Patterson Buckendahl, P ^a  

^a The State University of New Jersey   (United States)

Author keywords

Calcium binding protein; Dorsal root ganglia; Gamma carboxy glutamic acid; GPRC6A; Ionized calcium; Trigeminal ganglia; Uncarboxylated osteocalcin

Indexed keywords

BIOLOGICAL MARKER; CALCIUM; CALCIUM BINDING PROTEIN; CALCIUM ION; GLUTAMIC ACID; OSTEOCALCIN; RNA; VITAMIN K GROUP;

ARTICLE; BONE METABOLISM; BONE MINERAL; CALCIUM BINDING; CEREBELLUM; ENERGY METABOLISM; GENE EXPRESSION; HUMAN; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; MORPHOMETRICS; MOUSE MUTANT; NERVE CELL; NERVOUS SYSTEM; NONHUMAN; OSSIFICATION; OSTEOBLAST; PANCREAS ISLET BETA CELL; POLYMERASE CHAIN REACTION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SENSORY GANGLION; SIGNAL TRANSDUCTION; SPINAL GANGLION; STRESS; TRIGEMINAL NERVE;

ANIMALS; BONE AND BONES; CALCIUM; GANGLIA, SPINAL; MICE; MICE, KNOCKOUT; NEUROPEPTIDES; OSTEOCALCIN; PHYSICAL CONDITIONING, ANIMAL; RATS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 79961038700     PISSN: 12100668     EISSN: 13360329     Source Type: Journal    
DOI: 10.4149/endo_2011_02_99     Document Type: Article

References (67)

1. Banfi G, Lombardi G, Colombini A, Lippi G: Bone metabolism markers in sports medicine. Sports Med 40, 697-714, 2010. doi:10.2165/11533090-000000000-00000
2. Beresford JN, Gallagher JA, Poser JW, Russell RG: Production of osteocalcin by human bone cells in vitro. Effects of 1,25(OH)2D3, 24,25(OH)2D3, parathyroid hormone, and glucocorticoids. Metab Bone Dis Relat Res 5, 229-234, 1984. doi:10.1016/0221-8747(84)90064-X
3. Bloomfield SA, Mysiw WJ, Jackson RD: Bone mass and endocrine adaptations to training in spinal cord injured individuals. Bone 19, 61-68, 1996. doi:10.1016/8756-3282(96)00109-3
4. Cancela ML, Williamson MK, Price PA: Amino-acid sequence of bone Gla protein from the African clawed toad Xenopus laevis and the fish Sparus aurata. Int J Pept Protein Res 46, 419-423, 1995. doi:10.1111/j.1399-3011.1995.tb01076.x
5. Cavolina JM, Evans GL, Harris SA, Zhang M, Westerlind KC, Turner RT: The effects of orbital spaceflight on bone histomorphometry and messenger ribonucleic acid levels for bone matrix proteins and skeletal signaling peptides in ovariectomized growing rats. Endocrinology 138, 1567-1576, 1997. doi:10.1210/en.138.4.1567
6. Chrousos GP, Torpy DJ, Gold PW: Interactions between the hypothalamic-pituitary-adrenal axis and the female reproductive system: clinical implications. Ann Intern Med 129, 229-240, 1998.
7. Desbois C, Hogue DA, Karsenty G: The mouse osteocalcin gene cluster contains three genes with two separate spatial and temporal patterns of expression. J Biol Chem 269, 1183-1190, 1994.
8. Ducy P, Desbois C, Boyce B, Pinero G, Story B, Dunstan C, Smith E, Bonadio J, Goldstein S, Gundberg C, Bradley A, Karsenty G: Increased bone formation in osteocalcin-deficient mice. Nature 382, 448-452, 1996. doi:10.1038/382448a0
9. Ferron M, Hinoi E, Karsenty G, Ducy P: Osteocalcin differentially regulates beta cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci U S A 105, 5266-5270, 2008. doi:10.1073/pnas.0711119105
10. Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, Ducy P, Karsenty G: Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 142, 296-308, 2010. doi:10.1016/j.cell.2010.06.003
11. Fleet JC, Hock JM: Identification of osteocalcin mRNA in nonosteoid tissue of rats and humans by reverse transcription-polymerase chain reaction. J Bone Miner Res 9, 1565-1573, 1994. doi:10.1002/jbmr.5650091009
12. Frenkel B, Capparelli C, Van Auken M, Baran D, Bryan J, Stein JL, Stein GS, Lian JB: Activity of the osteocalcin promoter in skeletal sites of transgenic mice and during osteoblast differentiation in bone marrow-derived stromal cell cultures: effects of age and sex. Endocrinology 138, 2109-2116, 1997. doi:10.1210/en.138.5.2109
13. Fujita T, Ohgitani S, Nomura M: Fall of blood ionized calcium on watching a provocative TV program and its prevention by active absorbable algal calcium (AAA Ca). J Bone Miner Metab 17, 131-136, 1999. doi:10.1007/s007740050076
14. Globus RK, Bikle DD, Morey-Holton E: The temporal response of bone to unloading. Endocrinology 118, 733-742, 1986. doi:10.1210/endo-118-2-733
15. Guay A, Seftel AD, Traish A: Hypogonadism in men with erectile dysfunction may be related to a host of chronic illnesses. Int J Impot Res 22, 9-19, insert year!!! doi:10.1038/ijir.2009.46
16. Gundberg CM: Biochemical markers of bone formation. Clin Lab Med 20, 489-501, 2000.
17. Gundberg CM, Grant FD, Conlin PR, Chen CJ, Brown EM, Johnson PJ, LeBoff MS: Acute changes in serum osteocalcin during induced hypocalcemia in humans. J Clin Endocrinol Metab 72, 438-443, 1991. doi:10.1210/jcem-72-2-438
18. Hauschka PV, Henson EB, Gallop PM: Quantitative analysis and comparative decarboxylation of aminomalonic acid, beta-carboxyaspartic acid, and gamma-carboxyglutamic acid. Anal Biochem 108, 57-63, 1980. doi:10.1016/0003-2697(80)90691-0
19. Hauschka PV, Lian JB, Cole DE, Gundberg CM: Osteocalcin and matrix Gla protein: vitamin K- dependent proteins in bone. Physiol Rev 69, 990-1047, 1989.
20. Hauschka PV, Lian JB, Gallop PM: Direct identification of the calcium-binding amino acid, gamma- carboxyglutamate, in mineralized tissue. Proc Natl Acad Sci U S A 72, 3925-3929, 1975. doi:10.1073/pnas.72.10.3925
21. Hauschka PV, Reid ML: Vitamin D dependence of a calcium-binding protein containing gamma- carboxyglutamic acid in chicken bone. J Biol Chem 253, 9063-9068, 1978.
22. Hotchkiss CE, Brommage R, Du M, Jerome CP: The anesthetic isoflurane decreases ionized calcium and increases parathyroid hormone and osteocalcin in cynomolgus monkeys. Bone 23, 479-484, 1998. doi:10.1016/S8756-3282(98)00124-0
23. Ichikawa H, Itota T, Torii Y, Inoue K, Sugimoto T: Osteocalcin-immunoreactive primary sensory neurons in the rat spinal and trigeminal nervous systems. Brain Res 838, 205-209. 1999. doi:10.1016/S0006-8993(99)01710-2
24. Ichikawa H, Jin HW, Fujita M, Nagaoka N & Sugimoto T: Osteocalcin-immunoreactive neurons in the vagal and glossopharyngeal sensory ganglia of the rat. Brain Res 1031, 129-133. 2005. doi:10.1016/j.brainres.2004.10.011
25. Ichikawa H, Sugimoto T: The difference of osteocalcin-immunoreactive neurons in the rat dorsal root and trigeminal ganglia: co-expression with nociceptive transducers and central projection. Brain Res 958, 459-462, 2002. doi:10.1016/S0006-8993(02)03701-0
26. Jiang SD, Jiang LS, Dai LY: Spinal cord injury causes more damage to bone mass, bone structure, biomechanical properties and bone metabolism than sciatic neurectomy in young rats. Osteoporos Int 17, 1552-1561, 2006. doi:10.1007/s00198-006-0165-3
27. Kvetnansky R, Mikulaj L: Adrenal and urinary catecholamines in rats during adaptation to repeated immobilization stress. Endocrinology 87, 738-743, 1970. doi:10.1210/endo-87-4-738
28. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G: Endocrine regulation of energy metabolism by the skeleton. Cell 130, 456-469, 2007. doi:10.1016/j.cell.2007.05.047
29. Levinger I, Zebaze R, Jerums G, Hare DL, Selig S, Seeman E: The effect of acute exercise on undercarboxylated osteocalcin in obese men. Osteoporos Int., 22, 1621-1626, 2011.
30. Li YP, Stashenko P: Proinflammatory cytokines tumor necrosis factor-alpha and IL-6, but not IL- 1, down-regulate the osteocalcin gene promoter. J Immunol 148, 788-794, 1992.
31. Li YP, Stashenko P: Characterization of a tumor necrosis factor-responsive element which down- regulates the human osteocalcin gene. Mol Cell Biol 13, 3714-3721, 1993.
32. Lian JB, Stein GS, Stein JL, van Wijnen AJ: Osteocalcin gene promoter: unlocking the secrets for regulation of osteoblast growth and differentiation. J Cell Biochem Suppl 30-31, 62-72, 1998. doi:10.1002/(SICI)1097-4644(1998)72:30/31+<62::AID-JCB10>3.0.CO;2-S
33. Luo J, Liu Z, Liu J, Eugene CY: Distribution pattern of GPRC6A mRNA in mouse tissue by in situ hybridization. Zhong Nan Da Xue Xue Bao Yi Xue Ban 35, 1-10, 2010.
34. Macho L, Fickova M, Zorad S, Kvetnansky R: Changes of insulin binding in rat tissues after exposure to stress. Physiol Res 48, 51-58, 1999.
35. Macho L, Zorad S, Radikova Z, Patterson-Buckedahl P, Kvetnansky R: Ethanol consumption affects stress response and insulin binding in tissues of rats. Endocr Regul 37, 195-202, 2003.
36. Maimoun L, Manetta J, Couret I, Dupuy AM, Mariano-Goulart D, Micallef JP, Peruchon E, Rossi: The intensity level of physical exercise and the bone metabolism response. Int J Sports Med 27, 105-111, 2006.
37. Morey-Holton E, Globus RK, Kaplansky A, Durnova G: The hindlimb unloading rat model: literature overview, technique update and comparison with space flight data. Adv Space Biol Med 10, 7-40, 2005. doi:10.1016/S1569-2574(05)10002-1
38. Morey-Holton ER, Globus RK: Hindlimb unloading of growing rats: a model for predicting skeletal changes during space flight. Bone 22, 83S-88S, 1998. doi:10.1016/S8756-3282(98)00019-2
39. Morrison NA, Shine J, Fragonas JC, Verkest V, McMenemy ML, Eisman JA: 1,25- dihydroxyvitamin D-responsive element and glucocorticoid repression in the osteocalcin gene. Science 246, 1158-1161, 1989. doi:10.1126/science.2588000
40. Nelsestuen GL, Suttie JW: The mode of action of vitamin K. Isolation of a peptide containing the itamin K-dependent portion of prothrombin. Proc Natl Acad Sci USA 70, 3366-3370, 1973. doi:10.1073/pnas.70.12.3366
41. Nielsen HK, Laurberg P, Brixen K, Mosekilde L: Relations between diurnal variations in serum steocalcin, cortisol, parathyroid hormone, and ionized calcium in normal individuals. Acta Endocrinol (Copenh) 124, 391-398. 1991.
42. Oury F, Sumara G, Sumara O, Ferron M, Chang H, Smith CE, Hermo L, Suarez S, Roth BL, Ducy P, Arsenty G: Endocrine Regulation of Male Fertility by the Skeleton. Cell 144, 796-809, 2011.
43. Patterson-Buckendahl P, Arnaud SB, Mechanic GL, Martin RB, Grindeland RE, Cann CE: Fragility and composition of growing rat bone after one week in spaceflight. Am J Physiol 252, 240-246, 1987.
44. Patterson-Buckendahl P, Cann CE, Kvetnansky R: Osteocalcin Response to Stress - Is it a Stress Hormone? In Stress: Molecular Genetic and Neurobiological Advances, pp. 579-589. New York: Gordon and Breach Science, New York. 1996.
45. Patterson-Buckendahl P, Globus RK, Bikle DD, Cann CE & Morey-Holton E: Effects of simulated eightlessness on rat osteocalcin and bone calcium. Am J Physiol 257, R1103-R1109, 1989.
46. Patterson-Buckendahl P, Kubovcakova L, Krizanova O, Pohorecky LA, Kvetnansky R: Ethanol onsumption increases rat stress hormones and adrenomedullary gene expression. Alcohol 37, 157-166, 2005. doi:10.1016/j.alcohol.2005.09.007
47. Patterson-Buckendahl P, Kvetnansky R, Fukuhara K, Cizza G, Cann C: Regulation of plasma steocalcin by corticosterone and norepinephrine during restraint stress. Bone 17, 467-472, 1995. doi:10.1016/8756-3282(95)00281-X
48. Patterson-Buckendahl PE, Grindeland RE, Martin RB, Cann CE & Arnaud SB: Osteocalcin as an ndicator of bone metabolism during spaceflight. Physiologist 28, S227-S228, 1985.
49. Patterson-Buckendahl PE, Grindeland RE, Shakes DC, Morey-Holton ER, Cann CE: Circulating steocalcin in rats is inversely responsive to changes in corticosterone. Am J Physiol 254, R828-R833, 1988.
50. Pavy-Le Traon A, Heer M, Narici MV, Rittweger J, Vernikos J: From space to Earth: advances in uman physiology from 20 years of bed rest studies (1986-2006). Eur J Appl Physiol 101, 143-194, 2007. doi:10.1007/s00421-007-0474-z
51. Pi M, Chen L, Huang MZ, Zhu W, Ringhofer B, Luo J, Christenson L, Li B, Zhang J, Jackson PD, Faber P, Brunden KR, Harrington JJ, Quarles LD: GPRC6A null mice exhibit osteopenia, eminization and metabolic syndrome. PLoS One 3, e3858, 2008. doi:10.1371/journal.pone.0003858
52. Pi M, Faber P, Ekema G, Jackson PD, Ting A, Wang N, Fontilla-Poole M, Mays RW, Brunden KR, Harrington JJ, Quarles LD: Identification of a novel extracellular cation-sensing G-protein- coupled receptor. J Biol Chem 280, 40201-40209, 2005. doi:10.1074/jbc.M505186200
53. Poser JW, Price PA: A method for decarboxylation of gamma-carboxyglutamic acid in proteins. Properties of the decarboxylated gamma-carboxyglutamic acid protein from calf bone. J Biol Chem 254, 431-436, 1979.
54. Price PA, Otsuka AA, Poser JW, Kristaponis J, Raman N: Characterization of a gamma- carboxyglutamic acid-containing protein from bone. Proc Natl Acad Sci U S A 73, 1447-1451, 1976. doi:10.1073/pnas.73.5.1447
55. Riley V: Psychoneuroendocrine influences on immunocompetence and neoplasia. Science 212, 1100-1109, 1981. doi:10.1126/science.7233204
56. Roberts D, Lee W, Cuneo RC, Wittmann J, Ward G, Flatman R, McWhinney B, Hickman PE: Longitudinal study of bone turnover after acute spinal cord injury. J Clin Endocrinol Metab 83, 415-422, 1998. doi:10.1210/jc.83.2.415
57. Shackelford LC, LeBlanc AD, Driscoll TB, Evans HJ, Rianon NJ, Smith SM, Spector E, Feeback DL & Lai D: Resistance exercise as a countermeasure to disuse-induced bone loss. J Appl Physiol 97, 119-129, 2004. doi:10.1152/japplphysiol.00741.2003
58. Silver IA, Murrills RJ, Etherington DJ: Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts. Exp Cell Res 175, 266-276, 1988. doi:10.1016/0014-4827(88)90191-7
59. Stenflo J: Vitamin K and the biosynthesis of prothrombin. IV. Isolation of peptides containing prosthetic groups from normal prothrombin and the corresponding peptides from dicoumarol- induced prothrombin. J Biol Chem 249, 5527-5535, 1974.
60. Stenflo J, Fernlund P, Egan W, Roepstorff P: Vitamin K dependent modifications of glutamic acid residues in prothrombin. Proc Natl Acad Sci USA 71, 2730-2733, 1974. doi:10.1073/pnas.71.7.2730
61. Theofan G, Price PA: Bone Gla protein messenger ribonucleic acid is regulated by both 1,25- dihydroxyvitamin D3 and 3',5'-cyclic adenosine monophosphate in rat osteosarcoma cells. Mol Endocrinol 3, 36-43, 1989. doi:10.1210/mend-3-1-36
62. Thomas S, Movsowitz C, Epstein S, Jowell P, Ismail F: The response of circulating parameters of bone mineral metabolism to ethanol- and EDTA-induced hypocalcemia in the rat. Bone Miner 8, 1-6, 1990. doi:10.1016/0169-6009(91)90135-M
63. Wellendorph P, Brauner-Osborne H: Molecular cloning, expression, and sequence analysis of GPRC6A, a novel family C G-protein-coupled receptor. Gene 335, 37-46, 2004. doi:10.1016/j.gene.2004.03.003
64. Wellendorph P, Johansen LD, Jensen AA, Casanova E, Gassmann M, Deprez P, Clement-Lacroix P, Bettler B, Brauner-Osborne H: No evidence for a bone phenotype in GPRC6A knockout mice under normal physiological conditions. J Mol Endocrinol 42, 215-223, 2009. doi:10.1677/JME-08-0149
65. Xiao G, Jiang D, Ge C, Zhao Z, Lai Y, Boules H, Phimphilai M, Yang X, Karsenty G, Franceschi RT: Cooperative interactions between activating transcription factor 4 and Runx2/Cbfa1 stimulate osteoblast-specific osteocalcin gene expression. J Biol Chem 280, 30689-30696, 2005. doi:10.1074/jbc.M500750200
66. Xu F, Zhang J, Recio-Pinto E, Blanck TJ: Halothane and isoflurane augment depolarization-induced cytosolic CA2+ transients and attenuate carbachol-stimulated CA2+ transients. Anesthesiology 92, 1746-1756, 2000. doi:10.1097/00000542-200006000-00035
67. Yu S, Franceschi RT, Luo M, Zhang X, Jiang D, Lai Y, Jiang Y, Zhang J, Xiao G: Parathyroid hormone increases activating transcription factor 4 expression and activity in osteoblasts: requirement for osteocalcin gene expression. Endocrinology 149, 1960-1968, 2008. doi:10.1210/en.2007-1573