Expression of metastasin S100A4 is essential for bone resorption and regulates osteoclast function

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 2653-2663

  Erlandsson, Malin C ^a   Svensson, Mattias D ^a   Jonsson, Ing Marie ^a   Bian, Li ^a   Ambartsumian, Noona ^b   Andersson, Sofia ^a   Peng, ZhiQi ^c   Vääräniemi, Jukka ^c   Ohlsson, Claes ^a   Andersson, Karin M E ^a   Bokarewa, Maria I ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b Cancer Research Institute   (Denmark)

^c Pharmatest Ltd   (Finland)

Author keywords

Adhesion molecules; Bone; Cathepsin K; Osteoclasts; Osteopetrosis; S100A4

Indexed keywords

CALCIUM BINDING PROTEIN; CALVASCULIN; CATHEPSIN K; CELL ADHESION MOLECULE; COLLAGENASE 3; COLONY STIMULATING FACTOR 1; GELATINASE A; GELATINASE B; INTEGRIN; LENTIVIRUS VECTOR; OSTEOCALCIN; SHORT HAIRPIN RNA; STROMELYSIN;

ADHERENT CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE MARROW; BONE MARROW CELL; BONE MASS; BONE REMODELING; BONE STRENGTH; BONE TURNOVER; CELL DIFFERENTIATION; CELL MIGRATION; CHEMOKINESIS; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; CORTICAL BONE; FEMALE; GENE INACTIVATION; IMMUNOHISTOCHEMISTRY; LEUKOCYTE; MALE; MICRO-COMPUTED TOMOGRAPHY; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPOROSIS; PERIOSTEUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RHEUMATOID ARTHRITIS; THICKNESS; TRABECULAR BONE; TRANSCRIPTION REGULATION;

EID: 84881090366     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.06.020     Document Type: Article

References (48)

1. Boye K., Maelandsmo G.M. S100A4 and metastasis: a small actor playing many roles. Am. J. Pathol. 2010, 176:528-535.
2. Garrett S.C., Varney K.M., Weber D.J., Bresnick A.R. S100A4, a mediator of metastasis. J. Biol. Chem. 2006, 281:677-680.
3. Ford H.L., Silver D.L., Kachar B., Sellers J.R., Zain S.B. Effect of Mts1 on the structure and activity of nonmuscle myosin II. Biochemistry 1997, 36:16321-16327.
4. Kriajevska M., Fischer-Larsen M., Moertz E., Vorm O., Tulchinsky E., Grigorian M., Ambartsumian N., Lukanidin E. Liprin beta 1, a member of the family of LAR transmembrane tyrosine phosphatase-interacting proteins, is a new target for the metastasis-associated protein S100A4 (Mts1). J. Biol. Chem. 2002, 277:5229-5235.
5. Li Z.H., Spektor A., Varlamova O., Bresnick A.R. Mts1 regulates the assembly of nonmuscle myosin-IIA. Biochemistry 2003, 42:14258-14266.
6. Kim E.J., Helfman D.M. Characterization of the metastasis-associated protein, S100A4. Roles of calcium binding and dimerization in cellular localization and interaction with myosin. J. Biol. Chem. 2003, 278:30063-30073.
7. Berge G., Pettersen S., Grotterod I., Bettum I.J., Boye K., Maelandsmo G.M. Osteopontin-an important downstream effector of S100A4-mediated invasion and metastasis. Int. J. Cancer 2011, 129:780-790.
8. Schmidt-Hansen B., Ornas D., Grigorian M., Klingelhofer J., Tulchinsky E., Lukanidin E., Ambartsumian N. Extracellular S100A4 (Mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity. Oncogene 2004, 23:5487-5495.
9. Yammani R.R., Carlson C.S., Bresnick A.R., Loeser R.F. Increase in production of matrix metalloproteinase 13 by human articular chondrocytes due to stimulation with S100A4: role of the receptor for advanced glycation end products. Arthritis Rheum. 2006, 54:2901-2911.
10. Semov A., Moreno M.J., Onichtchenko A., Abulrob A., Ball M., Ekiel I., Pietrzynski G., Stanimirovic D., Alakhov V. Metastasis-associated protein S100A4 induces angiogenesis through interaction with Annexin II and accelerated plasmin formation. J. Biol. Chem. 2005, 280:20833-20841.
11. Oslejskova L., Grigorian M., Gay S., Neidhart M., Senolt L. The metastasis associated protein S100A4: a potential novel link to inflammation and consequent aggressive behaviour of rheumatoid arthritis synovial fibroblasts. Ann. Rheum. Dis. 2008, 67:1499-1504.
12. Senolt L., Grigorian M., Lukanidin E., Simmen B., Michel B.A., Pavelka K., Gay R.E., Gay S., Neidhart M. S100A4 is expressed at site of invasion in rheumatoid arthritis synovium and modulates production of matrix metalloproteinases. Ann. Rheum. Dis. 2006, 65:1645-1648.
13. Klingelhofer J., Senolt L., Baslund B., Nielsen G.H., Skibshoj I., Pavelka K., Neidhart M., Gay S., Ambartsumian N., Hansen B.S., Petersen J., Lukanidin E., Grigorian M. Up-regulation of metastasis-promoting S100A4 (Mts-1) in rheumatoid arthritis: putative involvement in the pathogenesis of rheumatoid arthritis. Arthritis Rheum. 2007, 56:779-789.
14. Senolt L., Grigorian M., Lukanidin E., Michel B.A., Gay R.E., Gay S., Pavelka K., Neidhart M. S100A4 (Mts1): is there any relation to the pathogenesis of rheumatoid arthritis?. Autoimmun. Rev. 2006, 5:129-131.
15. Erlandsson M.C., Forslind K., Andersson S.E., Lund A., Bokarewa M.I. Metastasin S100A4 is increased in proportion to radiographic damage in patients with RA. Rheumatology (Oxford) 2012, 51:932-940.
16. Bian L., Strzyz P., Jonsson I.M., Erlandsson M., Hellvard A., Brisslert M., Ohlsson C., Ambartsumian N., Grigorian M., Bokarewa M. S100A4 deficiency is associated with efficient bacterial clearance and protects against joint destruction during staphylococcal infection. J. Infect. Dis. 2011, 204:722-730.
17. Boyce B.F., Xing L. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch. Biochem. Biophys. 2008, 473:139-146.
18. Del Fattore A., Teti A., Rucci N. Osteoclast receptors and signaling. Arch. Biochem. Biophys. 2008, 473:147-160.
19. Lecaille F., Bromme D., Lalmanach G. Biochemical properties and regulation of cathepsin K activity. Biochimie 2008, 90:208-226.
20. Duarte W.R., Shibata T., Takenaga K., Takahashi E., Kubota K., Ohya K., Ishikawa I., Yamauchi M., Kasugai S. S100A4: a novel negative regulator of mineralization and osteoblast differentiation. J. Bone Miner. Res. 2003, 18:493-501.
21. Kato C., Kojima T., Komaki M., Mimori K., Duarte W.R., Takenaga K., Ishikawa I. S100A4 inhibition by RNAi up-regulates osteoblast related genes in periodontal ligament cells. Biochem. Biophys. Res. Commun. 2005, 326:147-153.
22. Sack U., Walther W., Scudiero D., Selby M., Aumann J., Lemos C., Fichtner I., Schlag P.M., Shoemaker R.H., Stein U. S100A4-induced cell motility and metastasis is restricted by the Wnt/beta-catenin pathway inhibitor calcimycin in colon cancer cells. Mol. Biol. Cell 2011, 22:3344-3354.
23. Stein U., Arlt F., Walther W., Smith J., Waldman T., Harris E.D., Mertins S.D., Heizmann C.W., Allard D., Birchmeier W., Schlag P.M., Shoemaker R.H. The metastasis-associated gene S100A4 is a novel target of beta-catenin/T-cell factor signaling in colon cancer. Gastroenterology 2006, 131:1486-1500.
24. Chen P.S., Wang M.Y., Wu S.N., Su J.L., Hong C.C., Chuang S.E., Chen M.W., Hua K.T., Wu Y.L., Cha S.T., Babu M.S., Chen C.N., Lee P.H., Chang K.J., Kuo M.L. CTGF enhances the motility of breast cancer cells via an integrin-alphavbeta3-ERK1/2-dependent S100A4-upregulated pathway. J. Cell Sci. 2007, 120:2053-2065.
25. Shen W., Chen D., Fu H., Liu S., Sun K., Sun X. S100A4 protects gastric cancer cells from anoikis through regulation of alphav and alpha5 integrin. Cancer Sci. 2011, 102:1014-1018.
26. Spiekerkoetter E., Guignabert C., de Jesus Perez V., Alastalo T.P., Powers J.M., Wang L., Lawrie A., Ambartsumian N., Schmidt A.M., Berryman M., Ashley R.H., Rabinovitch M. S100A4 and bone morphogenetic protein-2 codependently induce vascular smooth muscle cell migration via phospho-extracellular signal-regulated kinase and chloride intracellular channel 4. Circ. Res. 2009, 105:639-647. (613 pp. following 647).
27. Bjornland K., Winberg J.O., Odegaard O.T., Hovig E., Loennechen T., Aasen A.O., Fodstad O., Maelandsmo G.M. S100A4 involvement in metastasis: deregulation of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases in osteosarcoma cells transfected with an anti-S100A4 ribozyme. Cancer Res. 1999, 59:4702-4708.
28. Saleem M., Kweon M.H., Johnson J.J., Adhami V.M., Elcheva I., Khan N., Bin Hafeez B., Bhat K.M., Sarfaraz S., Reagan-Shaw S., Spiegelman V.S., Setaluri V., Mukhtar H. S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metalloproteinase 9. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:14825-14830.
29. Vu T.H., Shipley J.M., Bergers G., Berger J.E., Helms J.A., Hanahan D., Shapiro S.D., Senior R.M., Werb Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 1998, 93:411-422.
30. Naaman C.E.L., Grum-Schwensen B., Mansouri A., Grigorian M., Santoni-Rugiu E., Hansen T., Kriajevska M., Schafer B.W., Heizmann C.W., Lukanidin E., Ambartsumian N. Cancer predisposition in mice deficient for the metastasis-associated Mts1(S100A4) gene. Oncogene 2004, 23:3670-3680.
31. Ikonomidis J.S., Hendrick J.W., Parkhurst A.M., Herron A.R., Escobar P.G., Dowdy K.B., Stroud R.E., Hapke E., Zile M.R., Spinale F.G. Accelerated LV remodeling after myocardial infarction in TIMP-1-deficient mice: effects of exogenous MMP inhibition. Am. J. Physiol. Heart Circ. Physiol. 2005, 288:H149-H158.
32. Amu S., Gjertsson I., Brisslert M. Functional characterization of murine CD25 expressing B cells. Scand. J. Immunol. 2010, 71:275-282.
33. Windahl S.H., Vidal O., Andersson G., Gustafsson J.A., Ohlsson C. Increased cortical bone mineral content but unchanged trabecular bone mineral density in female ERbeta(-/-) mice. J. Clin. Invest. 1999, 104:895-901.
34. Parfitt A.M., Drezner M.K., Glorieux F.H., Kanis J.A., Malluche H., Meunier P.J., Ott S.M., Recker R.R. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 1987, 2:595-610.
35. Bostrom E.A., Svensson M., Andersson S., Jonsson I.M., Ekwall A.K., Eisler T., Dahlberg L.E., Smith U., Bokarewa M.I. Resistin and insulin/insulin-like growth factor signaling in rheumatoid arthritis. Arthritis Rheum. 2011, 63:2894-2904.
36. Elenjord R., Ljones H., Sundkvist E., Loennechen T., Winberg J.O. Dysregulation of matrix metalloproteinases and their tissue inhibitors by S100A4. Connect. Tissue Res. 2008, 49:185-188.
37. Roodman G.D. Regulation of osteoclast differentiation. Ann. N. Y. Acad. Sci. 2006, 1068:100-109.
38. Klingelhofer J., Ambartsumian N.S., Lukanidin E.M. Expression of the metastasis-associated Mts1 gene during mouse development. Dev. Dyn. 1997, 210:87-95.
39. Li Z.H., Dulyaninova N.G., House R.P., Almo S.C., Bresnick A.R. S100A4 regulates macrophage chemotaxis. Mol. Biol. Cell 2010, 21:2598-2610.
40. 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. The metastasis-associated Mts1(S100A4) protein could act as an angiogenic factor. Oncogene 2001, 20:4685-4695.
41. Miranda K.J., Loeser R.F., Yammani R.R. Sumoylation and nuclear translocation of S100A4 regulate IL-1beta-mediated production of matrix metalloproteinase-13. J. Biol. Chem. 2010, 285:31517-31524.
42. Krane S.M., Inada M. Matrix metalloproteinases and bone. Bone 2008, 43:7-18.
43. Stickens D., Behonick D.J., Ortega N., Heyer B., Hartenstein B., Yu Y., Fosang A.J., Schorpp-Kistner M., Angel P., Werb Z. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 2004, 131:5883-5895.
44. Lazner F., Gowen M., Pavasovic D., Kola I. Osteopetrosis and osteoporosis: two sides of the same coin. Hum. Mol. Genet. 1999, 8:1839-1846.
45. Frey J.B. What dwarfed Toulouse-Lautrec?. Nat. Genet. 1995, 10:128-130.
46. Saftig P., Hunziker E., Wehmeyer O., Jones S., Boyde A., Rommerskirch W., Moritz J.D., Schu P., von Figura K. Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13453-13458.
47. Everts V., Korper W., Hoeben K.A., Jansen I.D., Bromme D., Cleutjens K.B., Heeneman S., Peters C., Reinheckel T., Saftig P., Beertsen W. Osteoclastic bone degradation and the role of different cysteine proteinases and matrix metalloproteinases: differences between calvaria and long bone. J. Bone Miner. Res. 2006, 21:1399-1408.
48. Boissy P., Saltel F., Bouniol C., Jurdic P., Machuca-Gayet I. Transcriptional activity of nuclei in multinucleated osteoclasts and its modulation by calcitonin. Endocrinology 2002 May, 143(5):1913-1921.