Glutamate signaling in healthy and diseased bone

Frontiers in Endocrinology

Volumn 3, Issue JUL, 2012, Pages

  Cowan, Robert W ^a   Seidlitz, Eric P ^a   Singh, Gurmit ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Bone; Bone disease; Cancer; Glutamate; Homeostasis; Pathology; Rheumatoid arthritis; Signaling

Indexed keywords

EID: 84873607054     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2012.00089     Document Type: Short Survey

References (95)

1. Bannai, S. (1986). Exchange of cystine and glutamate across plasma membrane of human fibroblasts. J. Biol. Chem. 261, 2256-2263.
2. Berenson, J. R., Rajdev, L., and Broder, M. (2006). Pathophysiology of bone metastases. Cancer Biol. Ther. 5, 1078-1081.
3. Bleich, S., Romer, K., Wiltfang, J., and Kornhuber, J. (2003). Gluta- mate and the glutamate receptor system: a target for drug action. Int. J. Geriatr. Psychiatry 18(Suppl. 1), S33-S40.
4. Cammisotto, P. G., Gelinas, Y., Deshaies, Y., and Bukowiecki, L. J. (2005). Regulation of leptin secretion from white adipocytes by insulin, gly- colytic substrates, and amino acids. Am. J. Physiol. Endocrinol. Metab. 289, E166-E171.
5. Chenu, C., Serre, C. M., Raynal, C., Burt- Pichat, B., and Delmas, P. D. (1998). Glutamate receptors are expressed by bone cells and are involved in bone resorption. Bone 22, 295-299.
6. Chiu, J., DeSalle, R., Lam, H. M., Meisel, L., and Coruzzi, G. (1999). Molec- ular evolution of glutamate recep- tors: a primitive signaling mecha- nism that existed before plants and animals diverged. Mol. Biol. Evol. 16, 826-838.
7. Choi, K. Y., Chang, K., Pickel, J. M., Badger, J. D., and Roche, K. W. (2011). Expression of the metabotropic glutamate receptor 5 (mGluR5) induces melanoma in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 108, 15219-15224.
8. Davenport, R. (2002). Glutamate recep- tors in plants. Ann. Bot. 90, 549-557.
9. de Groot, J., and Sontheimer, H. (2011). Glutamate and the biology of gliomas. Glia 59, 1181-1189.
10. Dingledine, R., Borges, K., Bowie, D., and Traynelis, S. F. (1999). The glu- tamate receptor ion channels. Phar- macol. Rev. 51, 7-61.
11. Doxsee, D. W., Gout, P. W., Kurita, T., Lo, M., Buckley, A. R., Wang, Y., Xue, H., Karp, C. M., Cutz, J. C., Cunha, G. R., andWang, Y. Z. (2007). Sulfasalazine-induced cystine star- vation: potential use for prostate cancer therapy. Prostate 67, 162-171.
12. Ducy, P., Amling, M., Takeda, S., Priemel, M., Schilling, A. F., Beil, F. T., Shen, J., Vinson, C., Rueger, J. M., and Karsenty, G. (2000). Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 100, 197-207.
13. Elefteriou, F. (2008). Regulation of bone remodeling by the central and peripheral nervous system. Arch. Biochem. Biophys. 473, 231-236.
14. Elefteriou, F., Takeda, S., Liu, X., Armstrong, D., and Karsenty, G. (2003). Monosodium glutamate-sensitive hypothalamic neurons con- tribute to the control of bone mass. Endocrinology 144, 3842-3847.
15. Enz, R. (2007). The trick of the tail: protein-protein interactions of metabotropic glutamate receptors. Bioessays 29, 60-73.
16. Flood, S., Parri, R., Williams, A., Duance, V., and Mason, D. (2007). Modu- lation of interleukin-6 and matrix metalloproteinase 2 expression in human fibroblast-like synoviocytes by functional ionotropic gluta- mate receptors. Arthritis Rheum. 56, 2523-2534.
17. Genever, P. G., and Skerry, T. M. (2001). Regulation of spontaneous gluta- mate release activity in osteoblas- tic cells and its role in differentiation and survival: evidence for intrinsic glutamatergic signaling in bone. FASEB J. 15, 1586-1588.
18. Genever, P. G., Wilkinson, D. J., Pat- ton, A. J., Peet, N. M., Hong, Y., Mathur, A., Erusalimsky, J. D., and Skerry, T. M. (1999). Expression of a functional N-methyl-D-aspartate- type glutamate receptor by bone marrow megakaryocytes. Blood 93, 2876-2883.
19. Gu, X., Zhang, J., Ma, Z., Wang, J., Zhou, X., Jin, Y., Xia, X., Gao, Q., and Mei, F. (2010). The role of N-methyl-D- aspartate receptor subunit NR2B in spinal cord in cancer pain. Eur. J. Pain 14, 496-502.
20. Gu, Y., and Publicover, S. J. (2000). Expression of functional metabotropic glutamate receptors in primary cultured rat osteoblasts. Cross-talk with N-methyl-D- aspartate receptors. J. Biol. Chem. 275, 34252-34259.
21. Hajati, A. K., Alstergren, P., Näsström, K., Bratt, J., and Kopp, S. (2009). Endogenous glutamate in associa- tion with inflammatory and hor- monal factors modulates bone tis- sue resorption of the temporo- mandibular joint in patients with early rheumatoid arthritis. J. Oral Maxillofac. Surg. 67, 1895-1903.
22. Hajati, A. K., Näsström, K., Alstergren, P., Bratt, J., and Kopp, S. (2010). Temporomandibular joint bone tis- sue resorption in patients with early rheumatoid arthritis can be pre- dicted by joint crepitus and plasma glutamate level. Mediators Inflamm. 2010, 627803.
23. Hayashi, M., Morimoto, R., Yamamoto, A., and Moriyama, Y. (2003). Expres- sion and localization of vesicular glutamate transporters in pancreatic islets, upper gastrointestinal tract, and testis. J. Histochem. Cytochem. 51, 1375-1390.
24. Hinoi, E., Fujimori, S., Nakamura, Y., and Yoneda, Y. (2001). Group III metabotropic glutamate receptors in rat cultured calvarial osteoblasts. Biochem. Biophys. Res. Commun. 281, 341-346.
25. Hinoi, E., Fujimori, S., Takemori, A., Kurabayashi, H., Nakamura, Y., and Yoneda, Y. (2002). Demonstration of expression of mRNA for particular AMPA and kainate receptor subunits in immature and mature cultured rat calvarial osteoblasts. Brain Res. 943, 112-116.
26. Hinoi, E., Fujimori, S., and Yoneda, Y. (2003). Modulation of cellu- lar differentiation by N-methyl-D- aspartate receptors in osteoblasts. FASEB J. 17, 1532-1534.
27. Hinoi, E., Ohashi, R., Miyata, S., Kato, Y., Iemata, M., Hojo, H., Takarada, T., and Yoneda, Y. (2005). Exci- tatory amino acid transporters expressed by synovial fibroblasts in rats with collagen-induced arthritis. Biochem. Pharmacol. 70, 1744-1755.
28. Hinoi, E., Wang, L., Takemori, A., and Yoneda, Y. (2005). Functional expression of particular isoforms of excitatory amino acid transporters by rodent cartilage. Biochem. Phar- macol. 70, 70-81.
29. Hinoi, E., Takarada, T., Ueshima, T., Tsuchihashi, Y., and Yoneda, Y. (2004). Glutamate signaling in peripheral tissues. Eur. J. Biochem. 271, 1-13.
30. Hinoi, E., Takarada, T., and Yoneda, Y. (2004). Glutamate signaling sys- tem in bone. J. Pharmacol. Sci. 94, 215-220.
31. Hinoi, E., Takarada, T., Uno, K., Inoue, M., Murafuji, Y., and Yoneda, Y. (2007). Glutamate suppresses osteoclastogenesis through the cys- tine/glutamate antiporter. Am. J. Pathol. 170, 1277-1290.
32. Huggett, J. F., Mustafa, A., O'Neal, L., and Mason, D. J. (2002). The gluta- mate transporter GLAST-1 (EAAT- 1) is expressed in the plasma mem- brane of osteocytes and is responsive to extracellular glutamate concen- tration. Biochem. Soc. Trans. 30(Pt 6), 890-893.
33. Iemata, M., Takarada, T., Hinoi, E., Taniura, H., and Yoneda, Y. (2007). Suppression by glutamate of proliferative activity through glutathione depletion mediated by the cystine/glutamate antiporter in mesenchymal C3H10T1/2 stem cells. J. Cell. Physiol. 213, 721-729.
34. Itzstein, C., Cheynel, H., Burt-Pichat, B., Merle, B., Espinosa, L., Delmas, P. D., and Chenu, C. (2001). Molecular identification of NMDA glutamate receptors expressed in bone cells. J. Cell. Biochem. 82, 134-144.
35. Itzstein, C., Espinosa, L., Delmas, P. D., and Chenu, C. (2000). Spe- cific antagonists of NMDA recep- tors prevent osteoclast sealing zone formation required for bone resorp- tion. Biochem. Biophys. Res. Com- mun. 268, 201-209.
36. Kakegawa, W., Miyoshi, Y., Hamase, K., Matsuda, S., Matsuda, K., Kohda, K., Emi, K., Motohashi, J., Konno, R., Zaitsu, K., and Yuzaki, M. (2011). D- serine regulates cerebellar LTD and motor coordination through the δ2 glutamate receptor. Nat. Neurosci. 14, 603-611.
37. Kalariti, N., Lembessis, P., and Kout- silieris, M. (2004). Characteriza- tion of the glutamatergic system in MG-63 osteoblast-like osteosarcoma cells. Anticancer Res. 24, 3923-3929.
38. Kalariti, N., Lembessis, P., Papageor- giou, E., Pissimissis, N., and Kout- silieris, M. (2007). Regulation of the mGluR5, EAAT1 and GS expres- sion by glucocorticoids in MG-63 osteoblast-like osteosarcoma cells. J. Musculoskelet. Neuronal Interact. 7, 113-118.
39. Kim, J. Y., Kanai, Y., Chairoungdua, A., Cha, S. H., Matsuo, H., Kim, D. K., Inatomi, J., Sawa, H., Ida, Y., and Endou, H. (2001). Human cys- tine/glutamate transporter: cDNA cloning and upregulation by oxida- tive stress in glioma cells. Biochim. Biophys. Acta 1512, 335-344.
40. Krnjevic, K. (2010). When and why amino acids? J. Physiol. (Lond.) 588(Pt 1), 33-44.
41. Lam, F. F., and Ng, E. S. (2010). Substance P and glutamate recep- tor antagonists improve the anti- arthritic actions of dexamethasone in rats. Br. J. Pharmacol. 159, 958-969.
42. Lawand, N. B., Willis, W. D., and Westlund, K. N. (1997). Excitatory amino acid receptor involvement in peripheral nociceptive transmis- sion in rats. Eur. J. Pharmacol. 324, 169-177.
43. Liguz-Lecznar, M., and Skangiel- Kramska, J. (2007). Vesicular glutamate transporters (VGLUTs): the three musketeers of glutamater- gic system. Acta Neurobiol. Exp. (Wars) 67, 207-218.
44. Lin, T. H., Yang, R. S., Tang, C. H., Wu, M. Y., and Fu, W. M. (2008). Regula- tion of the maturation of osteoblasts and osteoclastogenesis by glutamate. Eur. J. Pharmacol. 589, 37-44.
45. Lindblad, S. S., Mydel, P., Hellvard, A., Jonsson, I. M., and Bokarewa, M. I. (2012). The N-methyl-d-aspartic acid receptor antagonist memantine ameliorates and delays the devel- opment of arthritis by enhancing regulatory T cells. Neurosignals 20, 61-71.
46. Lo, M., Wang, Y. Z., and Gout, P. W. (2008). The xc- cystine/glutamate antiporter: a potential target for therapy of cancer and other diseases. J. Cell. Physiol. 215, 593-602.
47. Marcaggi, P., Hirji, N., and Attwell, D. (2005). Release of L-aspartate by reversal of glutamate transporters. Neuropharmacology 49, 843-849.
48. Martin, T. J., and Seeman, E. (2008). Bone remodelling: its local reg- ulation and the emergence of bone fragility. Best Pract. Res. Clin. Endocrinol. Metab. 22, 701-722.
49. Mason, D. J., and Huggett, J. F. (2002). Glutamate transporters in bone. J. Musculoskelet. Neuronal Interact. 2, 406-414.
50. Mason, D. J., Suva, L. J., Genever, P. G., Patton, A. J., Steuckle, S., Hillam, R. A., and Skerry, T. M. (1997). Mechanically regulated expression of a neural glutamate transporter in bone: a role for excitatory amino acids as osteotropic agents? Bone 20, 199-205.
51. McNearney, T., Baethge, B. A., Cao, S., Alam, R., Lisse, J. R., and Westlund, K. N. (2004). Excitatory amino acids, TNF-α, and chemokine levels in syn- ovial fluids of patients with active arthropathies. Clin. Exp. Immunol. 137, 621-627.
52. McNearney, T., Speegle, D., Lawand, N., Lisse, J., and Westlund, K. N. (2000). Excitatory amino acid profiles of synovial fluid from patients with arthritis. J. Rheumatol. 27, 739-745.
53. Merle, B., Itzstein, C., Delmas, P. D., and Chenu, C. (2003). NMDA glutamate receptors are expressed by osteoclast precursors and involved in the reg- ulation of osteoclastogenesis. J. Cell. Biochem. 90, 424-436.
54. Miyaji, T., Omote, H., and Moriyama, Y. (2010). A vesicular transporter that mediates aspartate and glutamate neurotransmission. Biol. Pharm. Bull. 33, 1783-1785.
55. Morimoto, R., Uehara, S., Yatsushiro, S., Juge, N., Hua, Z., Senoh, S., Echigo, N., Hayashi, M., Mizoguchi, T., Ninomiya, T., Udagawa, N., Omote, H., Yamamoto, A., Edwards, R. H., and Moriyama, Y. (2006). Secre- tion of L-glutamate from osteoclasts through transcytosis. EMBO J. 25, 4175-4186.
56. Narang, V. S., Pauletti, G. M., Gout, P. W., Buckley, D. J., and Buckley, A. R. (2003). Suppression of cys- tine uptake by sulfasalazine inhibits proliferation of human mammary carcinoma cells. Anticancer Res. 23, 4571-4579.
57. Nedergaard, M., Takano, T., and Hansen, A. J. (2002). Beyond the role of glutamate as a neurotransmitter. Nat. Rev. Neurosci. 3, 748-755.
58. Niswender, C. M., and Conn, P. J. (2010). Metabotropic glutamate receptors: physiology, pharmacol- ogy, and disease. Annu. Rev. Phar- macol. Toxicol. 50, 295-322.
59. Olkku, A., Bodine, P. V., Linnala- Kankkunen, A., and Mahonen, A. (2004). Glucocorticoids induce glu- tamine synthetase expression in human osteoblastic cells: a novel observation in bone. Bone 34, 320-329.
60. Olkku, A., and Mahonen, A. (2008). Wnt and steroid pathways con- trol glutamate signalling by regulat- ing glutamine synthetase activity in osteoblastic cells. Bone 43, 483-493.
61. Olney, J. W. (1969). Brain lesions, obe- sity, and other disturbances in mice treated with monosodium gluta- mate. Science 164, 719-721.
62. Parisi, E., Almadén, Y., Ibarz, M., Panizo, S., Cardús, A., Rodriguez, M., Fernandez, E., and Valdivielso, J. M. (2009). N-methyl-D-aspartate receptors are expressed in rat parathyroid gland and regulate PTH secretion. Am. J. Physiol. Renal Phys- iol. 296, F1291-F1296.
63. Parisi, E., Bozic, M., Ibarz, M., Panizo, S., Valcheva, P., Coll, B., Fernández, E., and Valdivielso, J. M. (2010). Sus- tained activation of renal N-methyl- D-aspartate receptors decreases vit- amin D synthesis: a possible role for glutamate on the onset of secondary HPT. Am. J. Physiol. Endocrinol. Metab. 299, E825-E831.
64. Patton, A. J., Genever, P. G., Birch, M. A., Suva, L. J., and Skerry, T. M. (1998). Expression of an N-methyl- D-aspartate-type receptor by human and rat osteoblasts and osteoclasts suggests a novel glutamate signaling pathway in bone. Bone 22, 645-649.
65. Peet, N. M., Grabowski, P. S., Laketic- Ljubojevic, I., and Skerry, T. M. (1999). The glutamate receptor antagonist MK801 modulates bone resorption in vitro by a mechanism predominantly involving osteo- clast differentiation. FASEB J. 13, 2179-2185.
66. Piepoli, T., Mennuni, L., Zerbi, S., Lanza, M., Rovati, L. C., and Caselli, G. (2009). Glutamate signal- ing in chondrocytes and the poten- tial involvement of NMDA recep- tors in cell proliferation and inflam- matory gene expression. Osteoarthr. Cartil. 17, 1076-1083.
67. Ramage, L., Martel, M. A., Harding- ham, G. E., and Salter, D. M. (2008). NMDA receptor expression and activity in osteoarthritic human articular chondrocytes. Osteoarthr. Cartil. 16, 1576-1584.
68. Ren, B. X., Gu, X. P., Zheng, Y. G., Liu, C. L., Wang, D., Sun, Y. E., and Ma, Z. L. (2012). Intrathecal injection of metabotropic glutamate receptor subtype 3 and 5 agonist/antagonist attenuates bone cancer pain by inhi- bition of spinal astrocyte activation in a mouse model. Anesthesiology 116, 122-132.
69. Rzeski, W., Turski, L., and Ikonomi- dou, C. (2001). Glutamate antago- nists limit tumor growth. Proc. Natl. Acad. Sci. U.S.A. 98, 6372-6377.
70. Seidlitz, E. P., Sharma, M. K., Saikali, Z., Ghert, M., and Singh, G. (2009). Cancer cell lines release glutamate into the extracellular environment. Clin. Exp. Metastasis 26, 781-787.
71. Seidlitz, E. P., Sharma, M. K., and Singh, G. (2010). A by-product of glu- tathione production in cancer cells may cause disruption in bone meta- bolic processes. Can. J. Physiol. Phar- macol. 88, 197-203.
72. Seidlitz, E. P., Sharma, M. K., and Singh, G. (2010). Extracellular glu- tamate alters mature osteoclast and osteoblast functions. Can. J. Physiol. Pharmacol. 88, 929-936.
73. Sharma, M. K., Seidlitz, E. P., and Singh, G. (2010). Cancer cells release glutamate via the cystine/glutamate antiporter. Biochem. Biophys. Res. Commun. 391, 91-95.
74. Shigeri, Y., Seal, R. P., and Shimamoto, K. (2004). Molecular pharmacology of glutamate transporters, EAATs and VGLUTs. Brain Res. Brain Res. Rev. 45, 250-265.
75. Skerry, T. M. (2008). The role of gluta- mate in the regulation of bone mass and architecture. J. Musculoskelet. Neuronal Interact. 8, 166-173.
76. Skerry, T. M., and Genever, P. G. (2001). Glutamate signalling in non- neuronal tissues. Trends Pharmacol. Sci. 22, 174-181.
77. Sluka, K. A., Jordan, H. H., and West- lund, K. N. (1994). Reduction in joint swelling and hyperalgesia fol- lowing post-treatment with a non- NMDA glutamate receptor antago- nist. Pain 59, 95-100.
78. Spencer, G. J., Hitchcock, I. S., and Genever, P. G. (2004). Emerging neuroskeletal signalling pathways: a review. FEBS Lett. 559, 6-12.
79. Spencer, G. J., McGrath, C. J., and Gen- ever, P. G. (2007). Current perspec- tives on NMDA-type glutamate sig- nalling in bone. Int. J. Biochem. Cell Biol. 39, 1089-1104.
80. Stepulak, A., Luksch, H., Gebhardt, C., Uckermann, O., Marzahn, J., Sifringer, M., Rzeski, W., Staufner, C., Brocke, K. S., Turski, L., and Ikono- midou, C. (2009). Expression of glu- tamate receptor subunits in human cancers. Histochem. Cell Biol. 132, 435-445.
81. Suematsu, A., Tajiri, Y., Nakashima, T., Taka, J., Ochi, S., Oda, H., Nakamura, K., Tanaka, S., and Takayanagi, H. (2007). Scientific basis for the efficacy of combined use of antirheumatic drugs against bone destruction in rheumatoid arthritis. Mod. Rheumatol. 17, 17-23.
82. Szczesniak, A. M., Gilbert, R. W., Mukhida, M., and Anderson, G. I. (2005). Mechanical loading mod- ulates glutamate receptor subunit expression in bone. Bone 37, 63-73.
83. Takarada, T., Hinoi, E., Fujimori, S., Tsuchihashi, Y., Ueshima, T., Taniura, H., and Yoneda, Y. (2004). Accumulation of [3H] glutamate in cultured rat calvarial osteoblasts. Biochem. Pharmacol. 68, 177-184.
84. Takarada-Iemata, M., Takarada, T., Nakamura, Y., Nakatani, E., Hori, O., and Yoneda, Y. (2011). Glutamate preferentially suppresses osteoblas- togenesis than adipogenesis through the cystine/glutamate antiporter in mesenchymal stem cells. J. Cell. Physiol. 226, 652-665.
85. Takeda, S., Elefteriou, F., Levasseur, R., Liu, X., Zhao, L., Parker, K. L., Arm- strong, D., Ducy, P., and Karsenty, G. (2002). Leptin regulates bone for- mation via the sympathetic nervous system. Cell 111, 305-317.
86. Tanahashi, S., Ueda, Y., Nakajima, A., Yamamura, S., Nagase, H., and Okada, M. (2012). Novel δ1- receptor agonist KNT-127 increases the release of dopamine and L- glutamate in the striatum, nucleus accumbens and median pre-frontal cortex. Neuropharmacology 62, 2057-2067.
87. Taylor, A. F. (2002). Functional osteoblastic ionotropic glutamate receptors are a prerequisite for bone formation. J. Musculoskelet. Neuronal Interact. 2, 415-422.
88. Tremolizzo, L., DiFrancesco, J. C., Rodriguez-Menendez, V., Sir- tori, E., Longoni, M., Cassetti, A., Bossi, M., El Mestikawy, S., Cavaletti, G., and Ferrarese, C. (2006). Human platelets express the synaptic markers VGLUT1 and 2 and release glutamate following aggregation. Neurosci. Lett. 404, 262-265.
89. Tzingounis, A. V., and Wadiche, J. I. (2007). Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat. Rev. Neurosci. 8, 935-947.
90. Uno, K., Takarada, T., Nakamura, Y., Fujita, H., Hinoi, E., and Yoneda, Y. (2011). A negative correla- tion between expression profiles of runt-related transcription factor- 2 and cystine/glutamate antiporter xCT subunit in ovariectomized mouse bone. J. Pharmacol. Sci. 115, 309-319.
91. Waddell, T. G., and Miller, T. J. (1991). Chemical evolution of the citric acid cycle: sunlight photolysis of the amino acids glutamate and aspar- tate. Orig. Life Evol. Biosph. 21, 219-223.
92. Wang, L., Hinoi, E., Takemori, A., Nakamichi, N., and Yoneda, Y. (2006). Glutamate inhibits chondral mineralization through apoptotic cell death mediated by retrograde operation of the cystine/glutamate antiporter. J. Biol. Chem. 281, 24553-24565.
93. Watkins, J. C., and Jane, D. E. (2006). The glutamate story. Br. J. Pharma- col. 147(Suppl. 1), S100-S108.
94. Yamaki, M., Nakamura, H., Takahashi, N., Udagawa, N., and Ozawa, H. (2005). Transcytosis of calcium from bone by osteoclast-like cells evi- denced by direct visualization of cal- cium in cells.Arch. Biochem. Biophys. 440, 10-17.
95. Young, V. R., and Ajami, A. M. (2001). Glutamine: the emperor or his clothes? J. Nutr. 131(Suppl. 9), 2449S-2459S