Direct inhibitory and indirect stimulatory effects of RAGE ligand S100 on sRANKL-induced osteoclastogenesis

Journal of Cellular Biochemistry

Volumn 107, Issue 5, 2009, Pages 917-925

  Yoshida, Tomohiko ^a,b   Flegler, Ayanna ^a   Kozlov, Andrew ^a   Stern, Paula H ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Diabetes mellitus; Osteoclastogenesis; Rage (receptor of ages); S100 calgranulin family; S100a4 (MTS 1)

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; ALKALINE PHOSPHATASE; CALVASCULIN; COLONY STIMULATING FACTOR 1; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PROTEIN S 100;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; MINERALIZATION; MITOSIS INHIBITION; MULTINUCLEAR CELL; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TELOMERIC REPEAT AMPLIFICATION PROTOCOL;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HUMANS; LIGANDS; MACROPHAGES; MICE; MODELS, BIOLOGICAL; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; RANK LIGAND; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; S100 PROTEINS; SOLUBILITY;

EID: 67749106181     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22192     Document Type: Article

References (62)

1. Ambartsumian N, Klingelhofer J, Grigorian M, Christensen C, Kriajevska M, Tulchinsky E, Georgiev G, Berezin V, Bock E, Rygaard J, Cao R, Cao Y, Lukanidin E. 2001. The metastasis-associated Mts1(S100A4) protein could act as an angiogenic factor. Oncogene 20:4685-4695.
2. Bellows CG, Aubin JE, Heersche JN. 1991. Initiation and progression of mineralization of bone nodules formed in vitro: The role of alkaline phosphatase and organic phosphate. Bone Miner 14:27-40.
3. Boyle WJ, Simonet WS, Lacey DL. 2003. Osteoclast differentiation and activation. Nature 423:337-342.
4. Bucciarelli LG, Wendt T, Qu W, Lu Y, Lalla E, Rong LL, Goova MT, Moser B, Kislinger T, Lee DC, Kashyap Y, Stern DM, Schmidt AM. (2002a). RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice. Circulation 106:2827-2835.
5. Bucciarelli LG, Wendt T, Rong L, Lalla E, Hofmann MA, Goova MT, Taguchi A, Yan SF, Yan SD, Stern DM, Schmidt AM. (2002b). RAGE is a multiligand receptor of the immunoglobulin superfamily: Implications for homeostasis and chronic disease. Cell Mol Life Sci 59:1117-1128.
6. Chiarelli F, Giannini C, Mohn A. 2004. Growth, growth factors and diabetes. Eur J Endocrinol 151(Suppl. 3):U109-U117.
7. Cortizo AM, Lettieri MG, Barrio DA, Mercer N, Etcheverry SB, McCarthy AD. 2003. Advanced glycation end-products (AGEs) induce concerted changes in the osteoblastic expression of their receptor RAGE and in the activation of extracellular signal-regulated kinases (ERK). Mol Cell Biochem 250:1-10.
8. Davey GE, Murmann P, Heizmann CW. 2001. Intracellular Ca2+ and Zn2+ levels regulate the alternative cell density-dependent secretion of S100B in human glioblastoma cells. J Biol Chem 276:30819-30826.
9. Ding Q, Keller JN. (2005a). Evaluation of rage isoforms, ligands, and signaling in the brain. Biochim Biophys Acta 1746:18-27.
10. Ding Q, Keller JN. (2005b). Splice variants of the receptor for advanced glycosylation end products (RAGE) in human brain. Neurosci Lett 373:67-72.
11. Ding KH, Wang ZZ, Hamrick MW, Deng ZB, Zhou L, Kang B, Yan SL, She JX, Stern DM, Isales CM, Mi QS. 2006. Disordered osteoclast formation in RAGE-deficient mouse establishes an essential role for RAGE in diabetes related bone loss. Biochem Biophys Res Commun 340:1091-1097.
12. Donato R. 2003. Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60:540-551.
13. Duarte WR, Shibata T, Takenaga K, Takahashi E, Kubota K, Ohya K, Ishikawa I, Yamauchi M, Kasugai S. 2003. S100 A4: A novel negative regulator of mineralization and osteoblast differentiation. J Bone Miner Res 18:493-501.
14. Dukic-Stefanovic S, Gasic-Milenkovic J, Deuther-Conrad W, Munch G. 2003. Signal transduction pathways in mouse microglia N-11 cells activated by advanced glycation endproducts (AGEs). J Neurochem 87:44-55.
15. Ebralidze A, Tulchinsky E, Grigorian M, Afanasyeva A, Senin V, Revazova E, Lukanidin E. 1989. Isolation and characterization of a gene specifically expressed in different metastatic cells and whose deduced gene product has a high degree of homology to a Ca2+-binding protein family. Genes Dev 3:1086-1093.
16. Ecarot-Charrier B, Glorieux FH, van der Rest M, Pereira G. 1983. Osteoblasts isolated from mouse calvaria initiate matrix mineralization in culture. J Cell Biol 96:639-643.
17. Ecarot-Charrier B, Shepard N, Charette G, Grynpas M, Glorieux FH. 1988. Mineralization in osteoblast cultures: A light and electron microscopic study. Bone 9:147-154.
18. Ford HL, Zain SB. 1995. Interaction of metastasis associated Mts1 protein with nonmuscle myosin. Oncogene 10:1597-1605.
19. Franceschi RT, Iyer BS. 1992. Relationship between collagen synthesis and expression of the osteoblast phenotype in MC3T3-E1 cells. J Bone Miner Res 7:235-246.
20. Franceschi RT, Wilson JX, Dixon SJ. 1995. Requirement for Na(+)-dependent ascorbic acid transport in osteoblast function. Am J Physiol 268:C1430-C1439.
21. Gerstenfeld LC, Chipman SD, Glowacki J, Lian JB. 1987. Expression of differentiated function by mineralizing cultures of chicken osteoblasts. Dev Biol 122:49-60.
22. Grigorian MS, Tulchinsky EM, Zain S, Ebralidze AK, Kramerov DA, Kriajevska MV, Georgiev GP, Lukanidin EM. 1993. The mts1 gene and control of tumor metastasis. Gene 135:229-238.
23. Grigorian M, Andresen S, Tulchinsky E, Kriajevska M, Carlberg C, Kruse C, Cohn M, Ambartsumian N, Christensen A, Selivanova G, Lukanidin E. 2001. Tumor suppressor p53 protein is a new target for the metastasis-associated Mts1/S100A4 protein: Functional consequences of their interaction. J Biol Chem 276:22699-22708.
24. Hanford LE, Enghild JJ, Valnickova Z, Petersen SV, Schaefer LM, Schaefer TM, Reinhart TA, Oury TD. 2004. Purification and characterization of mouse soluble receptor for advanced glycation end products (sRAGE). J Biol Chem 279:50019-50024.
25. Haslbeck KM, Bierhaus A, Erwin S, Kirchner A, Nawroth P, Schlotzer U, Neundorfer B, Heuss D. 2004. Receptor for advanced glycation endproduct (RAGE)-mediated nuclear factor-kappaB activation in vasculitic neuropathy. Muscle Nerve 29:853-860.
26. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, Neurath MF, Slattery T, Beach D, McClary J, Nagashima M, Morser J, Stern D, Schmidt AM. 1999. RAGE mediates a novel proinflammatory axis: A central cell surface receptor for S100/calgranulin polypeptides. Cell 97:889-901.
27. Hu J, Castets F, Guevara JL, Van Eldik LJ. 1996. S100 beta stimulates inducible nitric oxide synthase activity and mRNA levels in rat cortical astrocytes. J Biol Chem 271:2543-2547.
28. Huang L, Xu J, Wood DJ, Zheng MH. 2000. Gene expression of osteoprotegerin ligand, osteoprotegerin, and receptor activator of NF-kappaB in giant cell tumor of bone: Possible involvement in tumor cell-induced osteoclastlike cell formation. Am J Pathol 156:761-767.
29. Huttunen HJ, Kuja-Panula J, Sorci G, Agneletti AL, Donato R, Rauvala H. 2000. Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation. J Biol Chem 275:40096-40105.
30. Ikeda T, Kasai M, Utsuyama M, Hirokawa K. 2001. Determination of three isoforms of the receptor activator of nuclear factor-kappaB ligand and their differential expression in bone and thymus. Endocrinology 142:1419-1426.
31. Kligman D, Marshak DR. 1985. Purification and characterization of a neurite extension factor from bovine brain. Proc Natl Acad Sci USA 82:7136-7139.
32. Kostenuik PJ, Shalhoub V. 2001. Osteoprotegerin: A physiological and pharmacological inhibitor of bone resorption. Curr Pharm Des 7:613-635.
33. Kriajevska MV, Cardenas MN, Grigorian MS, Ambartsumian NS, Georgiev GP, Lukanidin EM. 1994. Non-muscle myosin heavy chain as a possible target for protein encoded by metastasis-related mts-1 gene. J Biol Chem 269:19679-19682.
34. Li ZH, Spektor A, Varlamova O, Bresnick AR. 2003. Mts1 regulates the assembly of nonmuscle myosin-IIA. Biochemistry 42:14258-14266.
35. Li JH, Wang W, Huang XR, Oldfield M, Schmidt AM, Cooper ME, Lan HY. 2004. Advanced glycation end products induce tubular epithelial-myofibroblast transition through the RAGE-ERK1/2 MAP kinase signaling pathway. Am J Pathol 164:1389-1397.
36. McCarthy AD, Etcheverry SB, Cortizo AM. 1999. Advanced glycation endproduct-specific receptors in rat and mouse osteoblast-like cells: Regulation with stages of differentiation. Acta Diabetol 36:45-52.
37. Miyata T, Sprague SM. 1996. Advanced glycation of beta 2-microglobulin in the pathogenesis of bone lesions in dialysis-associated amyloidosis. Nephrol Dial Transplant 11(Suppl. 3):86-90.
38. Miyata T, Kawai R, Taketomi S, Sprague SM. 1996. Possible involvement of advanced glycation end-products in bone resorption. Nephrol Dial Transplant 11(Suppl. 5):54-57.
39. Motyl KJ, Botolin S, Irwin R, Appledorn DM, Kadakia T, Amalfitano A, Schwartz RC, McCabe LR. 2009. Bone inflammation and altered gene expression with type I diabetes early onset. J Cell Physiol 218:575-583.
40. Neeper M, Schmidt AM, Brett J, Yan SD, Wang F, Pan YC, Elliston K, Stern D, Shaw A. 1992. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem 267:14998-15004.
41. Nicodemus KK, Folsom AR. 2001. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192-1197.
42. Novitskaya V, Grigorian M, Kriajevska M, Tarabykina S, Bronstein I, Berezin V, Bock E, Lukanidin E. 2000. Oligomeric forms of the metastasis-related Mts1 (S100A4) protein stimulate neuronal differentiation in cultures of rat hippocampal neurons. J Biol Chem 275:41278-41286.
43. Okamoto T, Yamagishi S, Inagaki Y, Amano S, Koga K, Abe R, Takeuchi M, Ohno S, Yoshimura A, Makita Z. 2002. Angiogenesis induced by advanced glycation end products and its prevention by cerivastatin. FASEB J 16:1928-1930.
44. Park L, Raman KG, Lee KJ, Lu Y, Ferran LJ, Jr., Chow WS, Stern D, Schmidt AM. 1998. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat Med 4:1025-1031.
45. Pixley FJ, Stanley ER. 2004. CSF-1 regulation of the wandering macrophage: Complexity in action. Trends Cell Biol 14:628-638.
46. Qu Q, Perala-Heape M, Kapanen A, Dahllund J, Salo J, Vaananen HK, Harkonen P. 1998. Estrogen enhances differentiation of osteoblasts in mouse bone marrow culture. Bone 22:201-209.
47. Rammes A, Roth J, Goebeler M, Klempt M, Hartmann M, Sorg C. 1997. Myeloid-related protein (MRP) 8 and MRP14, calcium-binding proteins of the S100 family, are secreted by activated monocytes via a novel, tubulin-dependent pathway. J Biol Chem 272:9496-9502.
48. Rocken C, Kientsch-Engel R, Mansfeld S, Stix B, Stubenrauch K, Weigle B, Buhling F, Schwan M, Saeger W. 2003. Advanced glycation end products and receptor for advanced glycation end products in AA amyloidosis. Am J Pathol 162:1213-1220.
49. Schmidt AM, Yan SD, Yan SF, Stern DM. 2000. The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta 1498:99-111.
50. Schmidt AM, Yan SD, Yan SF, Stern DM. 2001. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 108:949-955.
51. Sousa MM, Yan SD, Stern D, Saraiva MJ. 2000. Interaction of the receptor for advanced glycation end products (RAGE) with transthyretin triggers nuclear transcription factor kB (NF-kB) activation. Lab Invest 80:1101-1110.
52. Suda T, Takahashi N, Udagawa N, Jimi E, Gillespie MT, Martin TJ. 1999. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 20:345-357.
53. Takagi M, Kasayama S, Yamamoto T, Motomura T, Hashimoto K, Yamamoto H, Sato B, Okada S, Kishimoto T. 1997. Advanced glycation endproducts stimulate interleukin-6 production by human bone-derived cells. J Bone Miner Res 12:439-446.
54. Thornalley PJ. 1998. Cell activation by glycated proteins. AGE receptors, receptor recognition factors and functional classification of AGEs. Cell Mol Biol (Noisy-le-grand) 44:1013-1023.
55. Van Eldik LJ, Zimmer DB. 1987. Secretion of S-100 from rat C6 glioma cells. Brain Res 436:367-370.
56. Vincent AM, Perrone L, Sullivan KA, Backus C, Sastry AM, Lastoskie C, Feldman EL. 2007. Receptor for advanced glycation end products activation injures primary sensory neurons via oxidative stress. Endocrinology 148:548-558.
57. Wear-Maggitti K, Lee J, Conejero A, Schmidt AM, Grant R, Breitbart A. 2004. Use of topical sRAGE in diabetic wounds increases neovascularization and granulation tissue formation. Ann Plast Surg 52:519-521 (discussion 522).
58. Winningham-Major F, Staecker JL, Barger SW, Coats S, Van Eldik LJ. 1989. Neurite extension and neuronal survival activities of recombinant S100 beta proteins that differ in the content and position of cysteine residues. J Cell Biol 109:3063-3071.
59. Yamamoto M, Yamaguchi T, Sugimoto T. 2006. Increased fracture rate in patients with type 2 diabetes mellitus is independent of its bone mineral density. Clin Calcium 16:1308-1314.
60. Yeh CH, Sturgis L, Haidacher J, Zhang XN, Sherwood SJ, Bjercke RJ, Juhasz O, Crow MT, Tilton RG, Denner L. 2001. Requirement for p38 and p44/p42 mitogen-activated protein kinases in RAGE-mediated nuclear factor-kappaB transcriptional activation and cytokine secretion. Diabetes 50:1495-1504.
61. Yoshida T, Asanuma M, Grossmann L, Fuse M, Shibata T, Yonekawa T, Tanaka T, Ueno K, Yasuda T, Saito Y, Tatsuno I. 2006. Geranylgeranylpyrophosphate (GGPP) synthase is down-regulated during differentiation of osteoblastic cell line MC3 T3-E1. FEBS Lett 580:5203-5207.
62. Zhou Z, Immel D, Xi CX, Bierhaus A, Feng X, Mei L, Nawroth P, Stern DM, Xiong WC. 2006. Regulation of osteoclast function and bone mass by RAGE. J Exp Med 203:1067-1080.