Acute-phase protein serum amyloid A3 is a novel paracrine coupling factor that controls bone homeostasis

FASEB Journal

Volumn 29, Issue 4, 2015, Pages 1344-1359

  Thaler, Roman ^a,b   Sturmlechner, Ines ^a   Spitzer, Silvia ^a   Riester, Scott M ^b   Rumpler, Monika ^a   Zwerina, Jochen ^a   Klaushofer, Klaus ^a   Van Wijnen, Andre J ^b   Varga, Franz ^a  

^a HANUSCH HOSPITAL   (Austria)

^b MAYO CLINIC   (United States)

Author keywords

Osteoblast; Osteoclast; Osteocyte; Osteogenesis

Indexed keywords

ACUTE PHASE PROTEIN; ALKALINE PHOSPHATASE; BONE GAMMA CARBOXYGLUTAMATE PROTEIN 2; CALCITONIN RECEPTOR; CATHEPSIN K; COLLAGEN TYPE 1; COLLAGEN TYPE 1 ALPHA 1; COLLAGENASE 3; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PURINERGIC P2X RECEPTOR; PURINERGIC P2X RECEPTOR 7; SCLEROSTIN; SERUM AMYLOID A; SERUM AMYLOID A1; SERUM AMYLOID A2; SERUM AMYLOID A3; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG; MMP13 PROTEIN, MOUSE; P2RX7 PROTEIN, MOUSE; PURINERGIC P2X7 RECEPTOR; SAA1 PROTEIN, HUMAN; SAA2 PROTEIN, HUMAN; SAA3 PROTEIN, MOUSE; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BONE HOMEOSTASIS; BONE MATURATION; BONE MINERALIZATION; CELL ACTIVITY; CELL COUNT; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL MATURATION; CONTROLLED STUDY; COUPLING FACTOR; ENZYME ACTIVATION; ENZYME REGULATION; ENZYME REPRESSION; EX VIVO STUDY; FEEDBACK SYSTEM; GENE MUTATION; GENE SILENCING; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NEGATIVE FEEDBACK; NEWBORN; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOSARCOMA CELL LINE; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; UPREGULATION; 3T3 CELL LINE; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE; BONE DEVELOPMENT; C57BL MOUSE; CELL CULTURE; CELL LINE; CYTOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; OSTEOBLAST; OSTEOCLAST; OSTEOCYTE; PARACRINE SIGNALING; SEQUENCE HOMOLOGY; SKULL;

3T3 CELLS; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, NEWBORN; BONE AND BONES; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; HOMEOSTASIS; HUMANS; MATRIX METALLOPROTEINASE 13; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; OSTEOBLASTS; OSTEOCALCIN; OSTEOCLASTS; OSTEOCYTES; OSTEOGENESIS; PARACRINE COMMUNICATION; PHYLOGENY; RECEPTORS, PURINERGIC P2X7; RNA, SMALL INTERFERING; SEQUENCE HOMOLOGY, AMINO ACID; SERUM AMYLOID A PROTEIN; SKULL;

EID: 84937393354     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-265512     Document Type: Article

References (70)

1. Li, X., and Cao, X. (2006) BMP signaling and skeletogenesis. Ann. N. Y. Acad. Sci. 1068, 26-40
2. Hadjidakis, D. J., and Androulakis, I. I. (2006) Bone remodeling. Ann. N. Y. Acad. Sci. 1092, 385-396
3. Kong, Y. Y., Yoshida, H., Sarosi, I., Tan, H. L., Timms, E., Capparelli, C., Morony, S., Oliveira-dos-Santos, A. J., Van, G., Itie, A., Khoo, W., Wakeham, A., Dunstan, C. R., Lacey, D. L., Mak, T. W., Boyle, W. J., and Penninger, J. M. (1999) OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397, 315-323
4. Del Fattore, A., Teti, A., and Rucci, N. (2012) Bone cells and the mechanisms of bone remodelling. Front Biosci. (Elite Ed.) 4, 2302-2321
5. Matsuoka, K., Park, K. A., Ito, M., Ikeda, K., and Takeshita, S. (2014) Osteoclast-derived complement component 3a stimulates osteoblast differentiation. J. Bone Miner. Res. 29, 1522-1530
6. Ryu, J., Kim, H. J., Chang, E. J., Huang, H., Banno, Y., and Kim, H. H. (2006) Sphingosine 1-phosphate as a regulator of osteoclast differentiation and osteoclast-osteoblast coupling. EMBO J. 25, 5840-5851
7. Dallas, S. L., and Bonewald, L. F. (2010) Dynamics of the transition from osteoblast to osteocyte. Ann. N. Y. Acad. Sci. 1192, 437-443
8. Nakashima, T., Hayashi, M., Fukunaga, T., Kurata, K., Oh-Hora, M., Feng, J. Q., Bonewald, L. F., Kodama, T., Wutz, A., Wagner, E. F., Penninger, J. M., and Takayanagi, H. (2011) Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat. Med. 17, 1231-1234
9. Bellido, T. (2014) Osteocyte-driven bone remodeling. Calcif. Tissue Int. 94, 25-34
10. Komori, T. (2014) Mouse models for the evaluation of osteocyte functions. J. Bone Metab. 21, 55-60
11. Price, J. S., Sugiyama, T., Galea, G. L., Meakin, L. B., Sunters, A., and Lanyon, L. E. (2011) Role of endocrine and paracrine factors in the adaptation of bone to mechanical loading. Curr. Osteoporos. Rep. 9, 76-82
12. Aubin, J. E., and Bonnelye, E. (2000) Osteoprotegerin and its ligand: a new paradigm for regulation of osteoclastogenesis and bone resorption. Osteoporos. Int. 11, 905-913
13. Lacey, D. L., Timms, E., Tan, H. L., Kelley, M. J., Dunstan, C. R., Burgess, T., Elliott, R., Colombero, A., Elliott, G., Scully, S., Hsu, H., Sullivan, J., Hawkins, N., Davy, E., Capparelli, C., Eli, A., Qian, Y. X., Kaufman, S., Sarosi, I., Shalhoub, V., Senaldi, G., Guo, J., Delaney, J., and Boyle, W. J. (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93, 165-176
14. Simonet, W. S., Lacey, D. L., Dunstan, C. R., Kelley, M., Chang, M. S., Lüthy, R., Nguyen, H. Q., Wooden, S., Bennett, L., Boone, T., Shimamoto, G., DeRose, M., Elliott, R., Colombero, A., Tan, H. L., Trail, G., Sullivan, J., Davy, E., Bucay, N., Renshaw-Gegg, L., Hughes, T. M., Hill, D., Pattison, W., Campbell, P., Sander, S., Van, G., Tarpley, J., Derby, P., Lee, R., and Boyle, W. J. (1997) Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89, 309-319
15. Winkler, D. G., Sutherland, M. K., Geoghegan, J. C., Yu, C., Hayes, T., Skonier, J. E., Shpektor, D., Jonas, M., Kovacevich, B. R., Staehling-Hampton, K., Appleby, M., Brunkow, M. E., and Latham, J. A. (2003) Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J. 22, 6267-6276
16. Van Bezooijen, R. L., ten Dijke, P., Papapoulos, S. E., and Löwik, C. W. (2005) SOST/sclerostin, an osteocyte-derived negative regulator of bone formation. Cytokine Growth Factor Rev. 16, 319-327
17. Paschalis, E. P., Tatakis, D. N., Robins, S., Fratzl, P., Manjubala, I., Zoehrer, R., Gamsjaeger, S., Buchinger, B., Roschger, A., Phipps, R., Boskey, A. L., Dall'Ara, E., Varga, P., Zysset, P., Klaushofer, K., and Roschger, P. (2011) Lathyrism-induced alterations in collagen cross-links influence the mechanical properties of bone material without affecting the mineral. Bone 49, 1232-1241
18. Thaler, R., Spitzer, S., Rumpler, M., Fratzl-Zelman, N., Klaushofer, K., Paschalis, E. P., and Varga, F. (2010) Differential effects of homocysteine and beta aminopropionitrile on preosteoblastic MC3T3-E1 cells. Bone 46, 703-709
19. Thaler, R., Zwerina, J., Rumpler, M., Spitzer, S., Gamsjaeger, S., Paschalis, E. P., Klaushofer, K., and Varga, F. (2013) Homocysteine induces serum amyloid A3 in osteoblasts via unlocking RGD-motifs in collagen. FASEB J. 27, 446-463
20. Uhlar, C. M., and Whitehead, A. S. (1999) Serum amyloid A, the major vertebrate acute-phase reactant. Eur. J. Biochem. 265, 501-523
21. Meek, R. L., Eriksen, N., and Benditt, E. P. (1992) Murine serum amyloid A3 is a high density apolipoprotein and is secreted by macrophages. Proc. Natl. Acad. Sci. USA 89, 7949-7952
22. Vallon, R., Freuler, F., Desta-Tsedu, N., Robeva, A., Dawson, J., Wenner, P., Engelhardt, P., Boes, L., Schnyder, J., Tschopp, C., Urfer, R., and Baumann, G. (2001) Serum amyloid A (apoSAA) expression is up-regulated in rheumatoid arthritis and induces transcription of matrix metalloproteinases. J. Immunol. 166, 2801-2807
23. Malle, E., and De Beer, F. C. (1996) Human serum amyloid A (SAA) protein: a prominent acute-phase reactant for clinical practice. Eur. J. Clin. Invest. 26, 427-435
24. Kumon, Y., Loose, L. D., Birbara, C. A., and Sipe, J. D. (1997) Rheumatoid arthritis exhibits reduced acute phase and enhanced constitutive serum amyloid A protein in synovial fluid relative to serum. A comparison with C-reactive protein. J. Rheumatol. 24, 14-19
25. Meek, R. L., and Benditt, E. P. (1986) Amyloid A gene family expression in different mouse tissues. J. Exp. Med. 164, 2006-2017
26. Thorn, C. F., Lu, Z. Y., and Whitehead, A. S. (2003) Tissue-specific regulation of the human acute-phase serum amyloid A genes, SAA1 and SAA2, by glucocorticoids in hepatic and epithelial cells. Eur. J. Immunol. 33, 2630-2639
27. Rygg, M., Nordstoga, K., Husby, G., and Marhaug, G. (1993) Expression of serum amyloid A genes in mink during induction of inflammation and amyloidosis. Biochim. Biophys. Acta 1216, 402-408
28. Subramanian, S., Han, C. Y., Chiba, T., McMillen, T. S., Wang, S. A., Haw III, A., Kirk, E. A., O'Brien, K. D., and Chait, A. (2008) Dietary cholesterol worsens adipose tissue macrophage accumulation and atherosclerosis in obese LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 28, 685-691
29. Zerega, B., Pagano, A., Pianezzi, A., Ulivi, V., Camardella, L., Cancedda, R., and Cancedda, F. D. (2004) Expression of serum amyloid A in chondrocytes and myoblasts differentiation and inflammation: possible role in cholesterol homeostasis. Matrix Biol. 23, 35-46
30. Chiba, T., Han, C. Y., Vaisar, T., Shimokado, K., Kargi, A., Chen, M. H., Wang, S., McDonald, T. O., O'Brien, K. D., Heinecke, J. W., and Chait, A. (2009) Serum amyloid A3 does not contribute to circulating SAA levels. J. Lipid Res. 50, 1353-1362
31. Reigstad, C. S., Lundén, G. O., Felin, J., and Bäckhed, F. (2009) Regulation of serum amyloid A3 (SAA3) in mouse colonic epithelium and adipose tissue by the intestinal microbiota. PLoS One 4, e5842
32. Sommer, G., Weise, S., Kralisch, S., Scherer, P. E., Lössner, U., Blüher, M., Stumvoll, M., and Fasshauer, M. (2008) The adipokine SAA3 is induced by interleukin-1beta in mouse adipocytes. J. Cell. Biochem. 104, 2241-2247
33. Maier, W., Altwegg, L. A., Corti, R., Gay, S., Hersberger, M., Maly, F. E., Sütsch, G., Roffi, M., Neidhart, M., Eberli, F. R., Tanner, F. C., Gobbi, S., von Eckardstein, A., and Lüscher, T. F. (2005) Inflammatory markers at the site of ruptured plaque in acute myocardial infarction: locally increased interleukin-6 and serum amyloid A but decreased C-reactive protein. Circulation 111, 1355-1361
34. Yamada, T., Wada, A., Itoh, K., and Igari, J. (2000) Serum amyloid A secretion from monocytic leukaemia cell line THP-1 and cultured human peripheral monocytes. Scand. J. Immunol. 52, 7-12
35. Han, C. Y., Subramanian, S., Chan, C. K., Omer, M., Chiba, T., Wight, T. N., and Chait, A. (2007) Adipocyte-derived serum amyloid A3 and hyaluronan play a role in monocyte recruitment and adhesion. Diabetes 56, 2260-2273
36. Westermark, G. T., Sletten, K., Grubb, A., and Westermark, P. (1990) AA-amyloidosis. Tissue component-specific association of various protein AA subspecies and evidence of a fourth SAA gene product. Am. J. Pathol. 137, 377-383
37. Cunnane, G. (2001) Amyloid precursors and amyloidosis in inflammatory arthritis. Curr. Opin. Rheumatol. 13, 67-73
38. Connolly, M., Veale, D. J., and Fearon, U. (2011) Acute serum amyloid A regulates cytoskeletal rearrangement, cell matrix interactions and promotes cell migration in rheumatoid arthritis. Ann. Rheum. Dis. 70, 1296-1303
39. Chung, T. F., Sipe, J. D., McKee, A., Fine, R. E., Schreiber, B. M., Liang, J. S., and Johnson, R. J. (2000) Serum amyloid A in Alzheimer's disease brain is predominantly localized to myelin sheaths and axonal membrane. Amyloid 7, 105-110
40. Katayama, T., Nakashima, H., Honda, Y., Suzuki, S., Yamamoto, T., Iwasaki, Y., and Yano, K. (2007) The relationship between acute phase serum amyloid A (SAA) protein concentrations and left ventricular systolic function in acute myocardial infarction patients treated with primary coronary angioplasty. Int. Heart J. 48, 45-55
41. Johnson, B. D., Kip, K. E., Marroquin, O. C., Ridker, P. M., Kelsey, S. F., Shaw, L. J., Pepine, C. J., Sharaf, B., Bairey Merz, C. N., Sopko, G., Olson, M. B., and Reis, S. E.; National Heart, Lung, and Blood Institute. (2004) Serum amyloid A as a predictor of coronary artery disease and cardiovascular outcome in women: the National Heart, Lung, and Blood Institute-Sponsored Women's Ischemia Syndrome Evaluation (WISE). Circulation 109, 726-732
42. Lewis, K. E., Kirk, E. A., McDonald, T. O., Wang, S., Wight, T. N., O'Brien, K. D., and Chait, A. (2004) Increase in serum amyloid a evoked by dietary cholesterol is associated with increased atherosclerosis in mice. Circulation 110, 540-545
43. Scheja, L., Heese, B., Zitzer, H., Michael, M. D., Siesky, A. M., Pospisil, H., Beisiegel, U., and Seedorf, K. (2008) Acute-phase serum amyloid A as a marker of insulin resistance in mice. Exp. Diabetes Res. 2008, 230837
44. Kovacevic, A., Hammer, A., Stadelmeyer, E., Windischhofer, W., Sundl, M., Ray, A., Schweighofer, N., Friedl, G., Windhager, R., Sattler, W., and Malle, E. (2008) Expression of serum amyloid A transcripts in human bone tissues, differentiated osteoblast-like stem cells and human osteosarcoma cell lines. J. Cell. Biochem. 103, 994-1004
45. Morris, A. G. (1981) Neoplastic transformation of mouse fibroblasts by murine sarcoma virus: a multi-step process. J. Gen. Virol. 53, 39-45
46. Walker, P. R., Boynton, A. L., and Whitfield, J. F. (1977) The inhibition by colchicine of the initiation of DNA synthesis by hepatocytes in regenerating rat liver and by cultivated WI-38 and C3H10T1/2 cells. J. Cell. Physiol. 93, 89-97
47. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
48. Thaler, R., Rumpler, M., Spitzer, S., Klaushofer, K., and Varga, F. (2011) Mospd1, a new player in mesenchymal versus epidermal cell differentiation. J. Cell. Physiol. 226, 2505-2515
49. Canalis, E. (2009) Growth factor control of bone mass. J. Cell. Biochem. 108, 769-777
50. Preciado-Patt, L., Hershkoviz, R., Fridkin, M., and Lider, O. (1996) Serum amyloid A binds specific extracellular matrix glycoproteins and induces the adhesion of resting CD4+ T cells. J. Immunol. 156, 1189-1195
51. Dallas, S. L., Rosser, J. L., Mundy, G. R., and Bonewald, L. F. (2002) Proteolysis of latent transforming growth factor-beta (TGF-beta) -binding protein-1 by osteoclasts. A cellular mechanism for release of TGF-beta from bone matrix. J. Biol. Chem. 277, 21352-21360
52. Niemi, K., Teirilä, L., Lappalainen, J., Rajamäki, K., Baumann, M. H., Öörni, K., Wolff, H., Kovanen, P. T., Matikainen, S., and Eklund, K. K. (2011) Serum amyloid A activates the NLRP3 inflammasome via P2X7 receptor and a cathepsin B-sensitive pathway. J. Immunol. 186, 6119-6128
53. Wesselius, A., Bours, M. J., Agrawal, A., Gartland, A., Dagnelie, P. C., Schwarz, P., and Jorgensen, N. R. (2011) Role of purinergic receptor polymorphisms in human bone. Front Biosci (Landmark Ed) 16, 2572-2585 (Elite Ed)
54. Pellegatti, P., Falzoni, S., Donvito, G., Lemaire, I., and Di Virgilio, F. (2011) P2X7 receptor drives osteoclast fusion by increasing the extracellular adenosine concentration. FASEB J. 25, 1264-1274
55. Syberg, S., Schwarz, P., Petersen, S., Steinberg, T. H., Jensen, J. E., Teilmann, J., and Jørgensen, N. R. (2012) Association between P2X7 Receptor Polymorphisms and Bone Status in Mice. J. Osteoporos. 2012, 637986
56. Im, H. J., Pacione, C., Chubinskaya, S., Van Wijnen, A. J., Sun, Y., and Loeser, R. F. (2003) Inhibitory effects of insulin-like growth factor-1 and osteogenic protein-1 on fibronectin fragment- and interleukin-1beta-stimulated matrix metalloproteinase-13 expression in human chondrocytes. J. Biol. Chem. 278, 25386-25394
57. Selvamurugan, N., Chou, W. Y., Pearman, A. T., Pulumati, M. R., and Partridge, N. C. (1998) Parathyroid hormone regulates the rat collagenase-3 promoter in osteoblastic cells through the cooperative interaction of the activator protein-1 site and the runt domain binding sequence. J. Biol. Chem. 273, 10647-10657
58. Boumah, C. E., Selvamurugan, N., and Partridge, N. C. (2005) Transcription in the osteoblast: regulatory mechanisms utilized by parathyroid hormone and transforming growth factor-beta. Prog. Nucleic Acid Res. Mol. Biol. 80, 287-321
59. Tang, S. Y., Herber, R. P., Ho, S. P., and Alliston, T. (2012) Matrix metalloproteinase-13 is required for osteocytic perilacunar remodeling and maintains bone fracture resistance. J. Bone Miner. Res. 27, 1936-1950
60. Pivetta, E., Scapolan, M., Pecolo, M., Wassermann, B., Abu-Rumeileh, I., Balestreri, L., Borsatti, E., Tripodo, C., Colombatti, A., and Spessotto, P. (2011) MMP-13 stimulates osteoclast differentiation and activation in tumour breast bone metastases. Breast Cancer Res. 13, R105
61. Betts, J. C., Edbrooke, M. R., Thakker, R. V., and Woo, P. (1991) The human acute-phase serum amyloid A gene family: structure, evolution and expression in hepatoma cells. Scand. J. Immunol. 34, 471-482
62. Sipe, J. (1999) Revised nomenclature for serum amyloid A (SAA). Nomenclature Committee of the International Society of Amyloidosis. Part 2. Amyloid 6, 67-70
63. Uhlar, C. M., Burgess, C. J., Sharp, P. M., and Whitehead, A. S. (1994) Evolution of the serum amyloid A (SAA) protein superfamily. Genomics 19, 228-235
64. Olsen, H. G., Skovgaard, K., Nielsen, O. L., Leifsson, P. S., Jensen, H. E., Iburg, T., and Heegaard, P. M. (2013) Organization and biology of the porcine serum amyloid A (SAA) gene cluster: isoform specific responses to bacterial infection. PLoS One 8, e76695
65. Den Hartigh, L. J., Wang, S., Goodspeed, L., Ding, Y., Averill, M., Subramanian, S., Wietecha, T., O'Brien, K. D., and Chait, A. (2014) Deletion of serum amyloid A3 improves high fat high sucrose diet-induced adipose tissue inflammation and hyperlipidemia in female mice. PLoS One 9, e108564
66. Jing, D., Baik, A. D., Lu, X. L., Zhou, B., Lai, X., Wang, L., Luo, E., and Guo, X. E. (2014) In situ intracellular calcium oscillations in osteocytes in intact mouse long bones under dynamic mechanical loading. FASEB J. 28, 1582-1592
67. Sun, D., Junger, W. G., Yuan, C., Zhang, W., Bao, Y., Qin, D., Wang, C., Tan, L., Qi, B., Zhu, D., Zhang, X., and Yu, T. (2013) Shockwaves induce osteogenic differentiation of human mesenchymal stem cells through ATP release and activation of P2X7 receptors. Stem Cells 31, 1170-1180
68. Armstrong, S., Pereverzev, A., Dixon, S. J., and Sims, S. M. (2009) Activation of P2X7 receptors causes isoform-specific translocation of protein kinase C in osteoclasts. J. Cell Sci. 122, 136-144
69. Holmbeck, K., Bianco, P., Pidoux, I., Inoue, S., Billinghurst, R. C., Wu, W., Chrysovergis, K., Yamada, S., Birkedal-Hansen, H., and Poole, A. R. (2005) The metalloproteinase MT1-MMP is required for normal development and maintenance of osteocyte processes in bone. J. Cell Sci. 118, 147-156
70. Karsdal, M. A., Hjorth, P., Henriksen, K., Kirkegaard, T., Nielsen, K. L., Lou, H., Delaissé, J. M., and Foged, N. T. (2003) Transforming growth factor-beta controls human osteoclastogenesis through the p38 MAPK and regulation of RANK expression. J. Biol. Chem. 278, 44975-44987