Abstract
The vast diversity of S100 proteins has demonstrated a multitude of biological correlations with cell growth, cell differentiation and cell survival in numerous physiological and pathological conditions in all cells of the body. This review summarises some of the reported regulatory functions of S100 proteins (namely S100A1, S100A2, S100A4, S100A6, S100A7, S100A8/S100A9, S100A10, S100A11, S100A12, S100B and S100P) on cellular migration and invasion, established in both culture and animal model systems and the possible mechanisms that have been proposed to be responsible. These mechanisms involve intracellular events and components of the cytoskeletal organisation (actin/myosin filaments, intermediate filaments and microtubules) as well as extracellular signalling at different cell surface receptors (RAGE and integrins). Finally, we shall attempt to demonstrate how aberrant expression of the S100 proteins may lead to pathological events and human disorders and furthermore provide a rationale to possibly explain why the expression of some of the S100 proteins (mainly S100A4 and S100P) has led to conflicting results on motility, depending on the cells used.
Similar content being viewed by others
Abbreviations
- EGF:
-
Epidermal growth factor
- F-actin:
-
Filamentous actin
- FGF:
-
Fibroblast growth factor
- G-actin:
-
Globular actin
- GAG:
-
Glycosaminoglycan
- IL:
-
Interleukin
- MMP:
-
Matrix metalloproteinases
- NM:
-
Non muscle myosin
- PMN:
-
Polymorphonuclear neutrophil
- RAGE:
-
Receptor for advanced glycation end product
- siRNA:
-
Small interfering RNA
- shRNA:
-
Short hairpin RNA
- TGF:
-
Transforming growth factor
- VEFG:
-
Vascular endothelial growth factor
References
Moore BW (1965) A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun 19(6):739–744
Donato R (2003) Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60(6):540–551. doi:10.1002/jemt.10296
Zimmer DB, Eubanks JO, Ramakrishnan D, Criscitiello MF (2012) Evolution of the S100 family of calcium sensor proteins. Cell Calcium 53(3):170–179. doi:10.1016/j.ceca.2012.11.006
Shang X, Cheng H, Zhou R (2008) Chromosomal mapping, differential origin and evolution of the S100 gene family. Genet Sel Evol GSE 40(4):449–464. doi:10.1051/gse:2008013
Barraclough R, Savin J, Dube SK, Rudland PS (1987) Molecular cloning and sequence of the gene for p9Ka. A cultured myoepithelial cell protein with strong homology to S-100, a calcium-binding protein. J Mol Biol 198(1):13–20
Donato R (1986) S-100 proteins. Cell Calcium 7(3):123–145
Gribenko AV, Makhatadze GI (1998) Oligomerization and divalent ion binding properties of the S100P protein: a Ca2+/Mg2+-switch model. J Mol Biol 283(3):679–694. doi:10.1006/jmbi.1998.2116
Barraclough R, Gibbs F, Smith JA, Haynes GA, Rudland PS (1990) Calcium-ion binding by the potential calcium-ion-binding protein, p9Ka. Biochem Biophys Res Commun 169(2):660–666
Strynadka NC, James MN (1989) Crystal structures of the helix-loop-helix calcium-binding proteins. Annu Rev Biochem 58:951–998. doi:10.1146/annurev.bi.58.070189.004511
Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS (2006) Calcium-dependent and -independent interactions of the S100 protein family. Biochem J 396(2):201–214. doi:10.1042/BJ20060195
Marenholz I, Heizmann CW, Fritz G (2004) S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 322(4):1111–1122. doi:10.1016/j.bbrc.2004.07.096
Donato R (1999) Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1450(3):191–231
Kligman D, Hilt DC (1988) The S100 protein family. Trends Biochem Sci 13(11):437–443. doi:10.1016/0968-0004(88)90218-6
Bhattacharya S, Bunick CG, Chazin WJ (2004) Target selectivity in EF-hand calcium binding proteins. Biochim Biophys Acta 1742(1–3):69–79. doi:10.1016/j.bbamcr.2004.09.002
Mohan SK, Yu C (2011) The IL1alpha-S100A13 heterotetrameric complex structure: a component in the non-classical pathway for interleukin 1alpha secretion. J Biol Chem 286(16):14608–14617. doi:10.1074/jbc.M110.201954
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(14):9496–9502
Forst B, Hansen MT, Klingelhofer J, Moller HD, Nielsen GH, Grum-Schwensen B, Ambartsumian N, Lukanidin E, Grigorian M (2010) Metastasis-inducing S100A4 and RANTES cooperate in promoting tumor progression in mice. PLoS ONE 5(4):e10374. doi:10.1371/journal.pone.0010374
Donato R, Sorci G, Riuzzi F, Arcuri C, Bianchi R, Brozzi F, Tubaro C, Giambanco I (2009) S100B’s double life: intracellular regulator and extracellular signal. Biochim Biophys Acta 1793(6):1008–1022. doi:10.1016/j.bbamcr.2008.11.009
Fritz G, Botelho HM, Morozova-Roche LA, Gomes CM (2010) Natural and amyloid self-assembly of S100 proteins: structural basis of functional diversity. FEBS J 277(22):4578–4590. doi:10.1111/j.1742-4658.2010.07887.x
Lukanidin E, Sleeman JP (2012) Building the niche: the role of the S100 proteins in metastatic growth. Semin Cancer Biol 22(3):216–225. doi:10.1016/j.semcancer.2012.02.006
Zimmer DB, Wright Sadosky P, Weber DJ (2003) Molecular mechanisms of S100-target protein interactions. Microsc Res Tech 60(6):552–559. doi:10.1002/jemt.10297
Sherbet GV (2009) Metastasis promoter S100A4 is a potentially valuable molecular target for cancer therapy. Cancer Lett 280(1):15–30. doi:10.1016/j.canlet.2008.10.037
Eckert RL, Broome AM, Ruse M, Robinson N, Ryan D, Lee K (2004) S100 proteins in the epidermis. J Invest Dermatol 123(1):23–33. doi:10.1111/j.0022-202X.2004.22719.x
He H, Li J, Weng S, Li M, Yu Y (2009) S100A11: diverse function and pathology corresponding to different target proteins. Cell Biochem Biophys 55(3):117–126. doi:10.1007/s12013-009-9061-8
Zimmer DB, Cornwall EH, Landar A, Song W (1995) The S100 protein family: history, function, and expression. Brain Res Bull 37(4):417–429
Moore BW, McGregor D (1965) Chromatographic and electrophoretic fractionation of soluble proteins of brain and liver. J Biol Chem 240:1647–1653
Haimoto H, Kato K (1987) S100a0 (alpha alpha) protein, a calcium-binding protein, is localized in the slow-twitch muscle fiber. J Neurochem 48(3):917–923
Wright NT, Cannon BR, Zimmer DB, Weber DJ (2009) S100A1: structure, function, and therapeutic potential. Curr Chem Biol 3(2):138–145. doi:10.2174/187231309788166460
Most P, Seifert H, Gao E, Funakoshi H, Volkers M, Heierhorst J, Remppis A, Pleger ST, DeGeorge BR Jr, Eckhart AD, Feldman AM, Koch WJ (2006) Cardiac S100A1 protein levels determine contractile performance and propensity toward heart failure after myocardial infarction. Circulation 114(12):1258–1268. doi:10.1161/CIRCULATIONAHA.106.622415
Most P, Lerchenmuller C, Rengo G, Mahlmann A, Ritterhoff J, Rohde D, Goodman C, Busch CJ, Laube F, Heissenberg J, Pleger ST, Weiss N, Katus HA, Koch WJ, Peppel K (2013) S100A1 deficiency impairs postischemic angiogenesis via compromised proangiogenic endothelial cell function and nitric oxide synthase regulation. Circ Res 112(1):66–78. doi:10.1161/CIRCRESAHA.112.275156
Wang G, Zhang S, Fernig DG, Martin-Fernandez M, Rudland PS, Barraclough R (2005) Mutually antagonistic actions of S100A4 and S100A1 on normal and metastatic phenotypes. Oncogene 24(8):1445–1454. doi:10.1038/sj.onc.1208291
Zimmer DB, Cornwall EH, Reynolds PD, Donald CM (1998) S100A1 regulates neurite organization, tubulin levels, and proliferation in PC12 cells. J Biol Chem 273(8):4705–4711
Sorci G, Agneletti AL, Donato R (2000) Effects of S100A1 and S100B on microtubule stability. An in vitro study using triton-cytoskeletons from astrocyte and myoblast cell lines. Neuroscience 99(4):773–783
Donato R, Isobe T, Okuyama T (1985) S-100 proteins and microtubules: analysis of the effects of rat brain S-100 (S-100b) and ox brain S-100a0, S-100a and S-100b on microtubule assembly-disassembly. FEBS Lett 186(1):65–69
Garbuglia M, Verzini M, Rustandi RR, Osterloh D, Weber DJ, Gerke V, Donato R (1999) Role of the C-terminal extension in the interaction of S100A1 with GFAP, tubulin, the S100A1- and S100B-inhibitory peptide, TRTK-12, and a peptide derived from p53, and the S100A1 inhibitory effect on GFAP polymerization. Biochem Biophys Res Commun 254(1):36–41. doi:10.1006/bbrc.1998.9881
Garbuglia M, Verzini M, Sorci G, Bianchi R, Giambanco I, Agneletti AL, Donato R (1999) The calcium-modulated proteins, S100A1 and S100B, as potential regulators of the dynamics of type III intermediate filaments. Brazilian J Med Biol Res Revista brasileira de pesquisas medicas e biologicas/Sociedade Brasileira de Biofisica [et al] 32(10):1177–1185
Garbuglia M, Verzini M, Giambanco I, Spreca A, Donato R (1996) Effects of calcium-binding proteins (S-100a(o), S-100a, S-100b) on desmin assembly in vitro. FASEB J Off Publ Fed Am Soc Exp Biol 10(2):317–324
Yamasaki R, Berri M, Wu Y, Trombitas K, McNabb M, Kellermayer MS, Witt C, Labeit D, Labeit S, Greaser M, Granzier H (2001) Titin-actin interaction in mouse myocardium: passive tension modulation and its regulation by calcium/S100A1. Biophys J 81(4):2297–2313. doi:10.1016/S0006-3495(01)75876-6
Fukushima H, Chung CS, Granzier H (2010) Titin-isoform dependence of titin-actin interaction and its regulation by S100A1/Ca2+ in skinned myocardium. J Biomed Biotechnol 2010:727239. doi:10.1155/2010/727239
Ritterhoff J, Most P (2012) Targeting S100A1 in heart failure. Gene Ther 19(6):613–621. doi:10.1038/gt.2012.8
Mandinova A, Atar D, Shäfer BW, Spiess M, Aebi U, Heizmann CW (1998) Distinct subcellular localization of calcium binding S100 proteins in human smooth muscle cells and their relocation in response to rises in intracellular calcium. J Cell Sci 111(Pt 14):2043–2054
Benfenati F, Ferrari R, Onofri F, Arcuri C, Giambanco I, Donato R (2004) S100A1 codistributes with synapsin I in discrete brain areas and inhibits the F-actin-bundling activity of synapsin I. J Neurochem 89(5):1260–1270. doi:10.1111/j.1471-4159.2004.02419.x
Nagy N, Brenner C, Markadieu N, Chaboteaux C, Camby I, Shäfer BW, Pochet R, Heizmann CW, Salmon I, Kiss R, Decaestecker C (2001) S100A2, a putative tumor suppressor gene, regulates in vitro squamous cell carcinoma migration. Lab Investig J Tech Meth Pathol 81(4):599–612
Tsai WC, Tsai ST, Jin YT, Wu LW (2006) Cyclooxygenase-2 is involved in S100A2-mediated tumor suppression in squamous cell carcinoma. Mol Cancer Res MCR 4(8):539–547. doi:10.1158/1541-7786.MCR-05-0266
Liu D, Rudland PS, Sibson DR, Platt-Higgins A, Barraclough R (2000) Expression of calcium-binding protein S100A2 in breast lesions. Br J Cancer 83(11):1473–1479. doi:10.1054/bjoc.2000.1488
Wolf S, Haase-Kohn C, Pietzsch J (2011) S100A2 in cancerogenesis: a friend or a foe? Amino Acids 41(4):849–861. doi:10.1007/s00726-010-0623-2
Nagy N, Hoyaux D, Gielen I, Shäfer BW, Pochet R, Heizmann CW, Kiss R, Salmon I, Decaestecker C (2002) The Ca2+-binding S100A2 protein is differentially expressed in epithelial tissue of glandular or squamous origin. Histol Histopathol 17(1):123–130
van Dieck J, Brandt T, Teufel DP, Veprintsev DB, Joerger AC, Fersht AR (2010) Molecular basis of S100 proteins interacting with the p53 homologs p63 and p73. Oncogene 29(14):2024–2035. doi:10.1038/onc.2009.490
Mueller A, Shäfer BW, Ferrari S, Weibel M, Makek M, Hochli M, Heizmann CW (2005) The calcium-binding protein S100A2 interacts with p53 and modulates its transcriptional activity. J Biol Chem 280(32):29186–29193. doi:10.1074/jbc.M505000200
Komada T, Araki R, Nakatani K, Yada I, Naka M, Tanaka T (1996) Novel specific chemtactic receptor for S100L protein on guinea pig eosinophils. Biochem Biophys Res Commun 220(3):871–874
Bulk E, Sargin B, Krug U, Hascher A, Jun Y, Knop M, Kerkhoff C, Gerke V, Liersch R, Mesters RM, Hotfilder M, Marra A, Koschmieder S, Dugas M, Berdel WE, Serve H, Muller-Tidow C (2009) S100A2 induces metastasis in non-small cell lung cancer. Clin Cancer Res 15(1):22–29. doi:10.1158/1078-0432.CCR-08-0953
Diederichs S, Bulk E, Steffen B, Ji P, Tickenbrock L, Lang K, Zanker KS, Metzger R, Schneider PM, Gerke V, Thomas M, Berdel WE, Serve H, Muller-Tidow C (2004) S100 family members and trypsinogens are predictors of distant metastasis and survival in early-stage non-small cell lung cancer. Cancer Res 64(16):5564–5569. doi:10.1158/0008-5472.CAN-04-2004
Naz S, Ranganathan P, Bodapati P, Shastry AH, Mishra LN, Kondaiah P (2012) Regulation of S100A2 expression by TGF-beta-induced MEK/ERK signalling and its role in cell migration/invasion. Biochem J 447(1):81–91. doi:10.1042/BJ20120014
Gimona M, Lando Z, Dolginov Y, Vandekerckhove J, Kobayashi R, Sobieszek A, Helfman DM (1997) Ca2+-dependent interaction of S100A2 with muscle and nonmuscle tropomyosins. J Cell Sci 110:611–621
Leclerc E, Fritz G, Vetter SW, Heizmann CW (2009) Binding of S100 proteins to RAGE: an update. Biochim Biophys Acta 1793(6):993–1007. doi:10.1016/j.bbamcr.2008.11.016
Davies BR, Davies MP, Gibbs FE, Barraclough R, Rudland PS (1993) Induction of the metastatic phenotype by transfection of a benign rat mammary epithelial cell line with the gene for p9Ka, a rat calcium-binding protein, but not with the oncogene EJ-ras-1. Oncogene 8(4):999–1008
Mishra SK, Siddique HR, Saleem M (2012) S100A4 calcium-binding protein is key player in tumor progression and metastasis: preclinical and clinical evidence. Cancer Metastasis Rev 31(1–2):163–172. doi:10.1007/s10555-011-9338-4
Rudland PS, Platt-Higgins A, Renshaw C, West CR, Winstanley JH, Robertson L, Barraclough R (2000) Prognostic significance of the metastasis-inducing protein S100A4 (p9Ka) in human breast cancer. Cancer Res 60(6):1595–1603
Boye K, Maelandsmo GM (2010) S100A4 and metastasis: a small actor playing many roles. Am J Pathol 176(2):528–535. doi:10.2353/ajpath.2010.090526
de Silva Rudland S, Platt-Higgins A, Winstanley JH, Jones NJ, Barraclough R, West C, Carroll J, Rudland PS (2011) Statistical association of basal cell keratins with metastasis-inducing proteins in a prognostically unfavorable group of sporadic breast cancers. Am J Pathol 179(2):1061–1072. doi:10.1016/j.ajpath.2011.04.022
Goh Then Sin C, Hersch N, Rudland PS, Barraclough R, Hoffmann B, Gross SR (2011) S100A4 downregulates filopodia formation through increased dynamic instability. Cell Adh Migr 5(5):439–447. doi:10.4161/cam.5.5.17773
Huang L, Xu Y, Cai G, Guan Z, Cai S (2012) Downregulation of S100A4 expression by RNA interference suppresses cell growth and invasion in human colorectal cancer cells. Oncol Rep 27(4):917–922. doi:10.3892/or.2011.1598
Li N, Song MM, Chen XH, Liu LH, Li FS (2012) S100A4 siRNA inhibits human pancreatic cancer cell invasion in vitro. Biomed Environ Sci BES 25(4):465–470. doi:10.3967/0895-3988.2012.04.012
Chen D, Zheng XF, Yang ZY, Liu DX, Zhang GY, Jiao XL, Zhao H (2012) S100A4 silencing blocks invasive ability of esophageal squamous cell carcinoma cells. World J Gastroenterol WJG 18(9):915–922. doi:10.3748/wjg.v18.i9.915
Wang L, Wang X, Liang Y, Diao X, Chen Q (2012) S100A4 promotes invasion and angiogenesis in breast cancer MDA-MB-231 cells by upregulating matrix metalloproteinase-13. Acta Biochim Pol 59(4):593–598
Bowers RR, Manevich Y, Townsend DM, Tew KD (2012) Sulfiredoxin redox-sensitive interaction with S100A4 and non-muscle myosin IIA regulates cancer cell motility. Biochemistry 51(39):7740–7754. doi:10.1021/bi301006w
Zhang K, Zhang M, Zhao H, Yan B, Zhang D, Liang J (2012) S100A4 regulates motility and invasiveness of human esophageal squamous cell carcinoma through modulating the AKT/Slug signal pathway. Dis Esophagus Off J Int Soc Dis Esophagus/ISDE 25(8):731–739. doi:10.1111/j.1442-2050.2012.01323.x
Sack U, Walther W, Scudiero D, Selby M, Aumann J, Lemos C, Fichtner I, Schlag PM, Shoemaker RH, Stein U (2011) S100A4-induced cell motility and metastasis is restricted by the Wnt/beta-catenin pathway inhibitor calcimycin in colon cancer cells. Mol Biol Cell 22(18):3344–3354. doi:10.1091/mbc.E10-09-0739
Jenkinson SR, Barraclough R, West CR, Rudland PS (2004) S100A4 regulates cell motility and invasion in an in vitro model for breast cancer metastasis. Br J Cancer 90(1):253–262. doi:10.1038/sj.bjc.6601483
Hapangama DK, Raju RS, Valentijn AJ, Barraclough D, Hart A, Turner MA, Platt-Higgins A, Barraclough R, Rudland PS (2012) Aberrant expression of metastasis-inducing proteins in ectopic and matched eutopic endometrium of women with endometriosis: implications for the pathogenesis of endometriosis. Hum Reprod 27(2):394–407. doi:10.1093/humrep/der412
Rudland PS, Barraclough R, Fernig DG, Smith JA (1998) Growth and differentiation of the normal mammary gland and its tumours. Biochem Soc Symp 63:1–20
Barraclough R, Dawson KJ, Rudland PS (1982) Control of protein synthesis in cuboidal rat mammary epithelial cells in culture. Changes in gene expression accompany the formation of elongated cells. Eur J Biochem 129(2):335–341
Andersen K, Mori H, Fata J, Bascom J, Oyjord T, Maelandsmo GM, Bissell M (2011) The metastasis-promoting protein S100A4 regulates mammary branching morphogenesis. Dev Biol 352(2):181–190. doi:10.1016/j.ydbio.2010.12.033
Gibbs FE, Barraclough R, Platt-Higgins A, Rudland PS, Wilkinson MC, Parry EW (1995) Immunocytochemical distribution of the calcium-binding protein p9Ka in normal rat tissues: variation in the cellular location in different tissues. J Histochem Cytochem 43(2):169–180
Grigorian M, Tulchinsky E, Burrone O, Tarabykina S, Georgiev G, Lukanidin E (1994) Modulation of mts1 expression in mouse and human normal and tumor cells. Electrophoresis 15(3–4):463–468
Takenaga K, Nakamura Y, Sakiyama S (1994) Cellular localization of pEL98 protein, an S100-related calcium binding protein, in fibroblasts and its tissue distribution analyzed by monoclonal antibodies. Cell Struct Funct 19(3):133–141
Jackson-Grusby LL, Swiergiel J, Linzer DI (1987) A growth-related mRNA in cultured mouse cells encodes a placental calcium binding protein. Nucl Acids Res 15(16):6677–6690
Davies M, Harris S, Rudland P, Barraclough R (1995) Expression of the rat, S-100-related, calcium-binding protein gene, p9Ka, in transgenic mice demonstrates different patterns of expression between these two species. DNA Cell Biol 14(10):825–832
EL Naaman C, Grum-Schwensen B, Mansouri A, Grigorian M, Santoni-Rugiu E, Hansen T, Kriajevska M, Shäfer BW, Heizmann CW, Lukanidin E, Ambartsumian N (2004) Cancer predisposition in mice deficient for the metastasis-associated Mts1(S100A4) gene. Oncogene 23(20):3670–3680. doi:10.1038/sj.onc.1207420
Davies MP, Rudland PS, Robertson L, Parry EW, Jolicoeur P, Barraclough R (1996) Expression of the calcium-binding protein S100A4 (p9Ka) in MMTV-neu transgenic mice induces metastasis of mammary tumours. Oncogene 13(8):1631–1637
Li ZH, Dulyaninova NG, House RP, Almo SC, Bresnick AR (2010) S100A4 regulates macrophage chemotaxis. Mol Biol Cell 21(15):2598–2610. doi:10.1091/mbc.E09-07-0609
Strutz F, Okada H, Lo CW, Danoff T, Carone RL, Tomaszewski JE, Neilson EG (1995) Identification and characterization of a fibroblast marker: FSP1. J Cell Biol 130(2):393–405
Okada H, Danoff TM, Kalluri R, Neilson EG (1997) Early role of Fsp1 in epithelial–mesenchymal transformation. Am J Physiol 273(4 Pt 2):F563–F574
Schneider M, Hansen JL, Sheikh SP (2008) S100A4: a common mediator of epithelial-mesenchymal transition, fibrosis and regeneration in diseases? J Mol Med (Berl) 86(5):507–522. doi:10.1007/s00109-007-0301-3
Xue C, Plieth D, Venkov C, Xu C, Neilson EG (2003) The gatekeeper effect of epithelial–mesenchymal transition regulates the frequency of breast cancer metastasis. Cancer Res 63(12):3386–3394
Li ZH, Bresnick AR (2006) The S100A4 metastasis factor regulates cellular motility via a direct interaction with myosin-IIA. Cancer Res 66(10):5173–5180. doi:10.1158/0008-5472.CAN-05-3087
Malashkevich VN, Varney KM, Garrett SC, Wilder PT, Knight D, Charpentier TH, Ramagopal UA, Almo SC, Weber DJ, Bresnick AR (2008) Structure of Ca2+-bound S100A4 and its interaction with peptides derived from nonmuscle myosin-IIA. Biochemistry 47(18):5111–5126. doi:10.1021/bi702537s
Semov A, Moreno MJ, Onichtchenko A, Abulrob A, Ball M, Ekiel I, Pietrzynski G, Stanimirovic D, Alakhov V (2005) Metastasis-associated protein S100A4 induces angiogenesis through interaction with Annexin II and accelerated plasmin formation. J Biol Chem 280(21):20833–20841. doi:10.1074/jbc.M412653200
Cabezon T, Celis JE, Skibshoj I, Klingelhofer J, Grigorian M, Gromov P, Rank F, Myklebust JH, Maelandsmo GM, Lukanidin E, Ambartsumian N (2007) Expression of S100A4 by a variety of cell types present in the tumor microenvironment of human breast cancer. Int J Cancer 121(7):1433–1444. doi:10.1002/ijc.22850
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(34):4685–4695. doi:10.1038/sj.onc.1204636
Lawrie A, Spiekerkoetter E, Martinez EC, Ambartsumian N, Sheward WJ, MacLean MR, Harmar AJ, Schmidt AM, Lukanidin E, Rabinovitch M (2005) Interdependent serotonin transporter and receptor pathways regulate S100A4/Mts1, a gene associated with pulmonary vascular disease. Circ Res 97(3):227–235. doi:10.1161/01.RES.0000176025.57706.1e
Spiekerkoetter E, Guignabert C, de Jesus Perez V, Alastalo TP, Powers JM, Wang L, Lawrie A, Ambartsumian N, Schmidt AM, Berryman M, Ashley RH, Rabinovitch M (2009) 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 105(7):639–647, 613 p following 647. doi:10.1161/CIRCRESAHA.109.205120
Klingelhofer J, Grum-Schwensen B, Beck MK, Knudsen RS, Grigorian M, Lukanidin E, Ambartsumian N (2012) Anti-S100A4 antibody suppresses metastasis formation by blocking stroma cell invasion. Neoplasia 14(12):1260–1268
Schmidt-Hansen B, Ornas D, Grigorian M, Klingelhofer J, Tulchinsky E, Lukanidin E, Ambartsumian N (2004) Extracellular S100A4(mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity. Oncogene 23(32):5487–5495. doi:10.1038/sj.onc.1207720
Takenaga K, Kozlova EN (2006) Role of intracellular S100A4 for migration of rat astrocytes. Glia 53(3):313–321. doi:10.1002/glia.20284
Fang Z, Duthoit N, Wicher G, Kallskog O, Ambartsumian N, Lukanidin E, Takenaga K, Kozlova EN (2006) Intracellular calcium-binding protein S100A4 influences injury-induced migration of white matter astrocytes. Acta Neuropathol 111(3):213–219. doi:10.1007/s00401-005-0019-7
Dmytriyeva O, Pankratova S, Owczarek S, Sonn K, Soroka V, Ridley CM, Marsolais A, Lopez-Hoyos M, Ambartsumian N, Lukanidin E, Bock E, Berezin V, Kiryushko D (2012) The metastasis-promoting S100A4 protein confers neuroprotection in brain injury. Nature communications 3:1197. doi:10.1038/ncomms2202
Takenaga K, Nakamura Y, Sakiyama S, Hasegawa Y, Sato K, Endo H (1994) Binding of pEL98 protein, an S100-related calcium-binding protein, to nonmuscle tropomyosin. J Cell Biol 124(5):757–768
Watanabe Y, Usada N, Minami H, Morita T, Tsugane S, Ishikawa R, Kohama K, Tomida Y, Hidaka H (1993) Calvasculin, as a factor affecting the microfilament assemblies in rat fibroblasts transfected by src gene. FEBS Lett 324(1):51–55
Flynn AM, Rudland PS, Barraclough R (1996) Protein interactions between S100A4 (p9Ka) and other cellular proteins identified using in vitro methods. Biochem Soc Trans 24(3):341S
Chen H, Fernig DG, Rudland PS, Sparks A, Wilkinson MC, Barraclough R (2001) Binding to intracellular targets of the metastasis-inducing protein, S100A4 (p9Ka). Biochem Biophys Res Commun 286(5):1212–1217. doi:10.1006/bbrc.2001.5517
Chen M, Bresnick AR, O’Connor KL (2012) Coupling S100A4 to Rhotekin alters Rho signaling output in breast cancer cells. Oncogene (Epub ahead of print). doi:10.1038/onc.2012.383
Fukata Y, Oshiro N, Kinoshita N, Kawano Y, Matsuoka Y, Bennett V, Matsuura Y, Kaibuchi K (1999) Phosphorylation of adducin by Rho-kinase plays a crucial role in cell motility. J Cell Biol 145(2):347–361
O’Connor KL, Nguyen BK, Mercurio AM (2000) RhoA function in lamellae formation and migration is regulated by the alpha6beta4 integrin and cAMP metabolism. J Cell Biol 148(2):253–258
Kurokawa K, Matsuda M (2005) Localized RhoA activation as a requirement for the induction of membrane ruffling. Mol Biol Cell 16(9):4294–4303. doi:10.1091/mbc.E04-12-1076
Petrie RJ, Yamada KM (2013) At the leading edge of three-dimensional cell migration. J Cell Sci 125(Pt 24):5917–5926. doi:10.1242/jcs.093732
Sudo K, Ito H, Iwamoto I, Morishita R, Asano T, Nagata K (2006) Identification of a cell polarity-related protein, Lin-7B, as a binding partner for a Rho effector, Rhotekin, and their possible interaction in neurons. Neurosci Res 56(4):347–355. doi:10.1016/j.neures.2006.08.003
Li ZH, Spektor A, Varlamova O, Bresnick AR (2003) Mts1 regulates the assembly of nonmuscle myosin-IIA. Biochemistry 42(48):14258–14266. doi:10.1021/bi0354379
Dulyaninova NG, Malashkevich VN, Almo SC, Bresnick AR (2005) Regulation of myosin-IIA assembly and Mts1 binding by heavy chain phosphorylation. Biochemistry 44(18):6867–6876. doi:10.1021/bi0500776
Ford HL, Silver DL, Kachar B, Sellers JR, Zain SB (1997) Effect of Mts1 on the structure and activity of nonmuscle myosin II. Biochemistry 36(51):16321–16327. doi:10.1021/bi971182l
Parsons JT, Horwitz AR, Schwartz MA (2010) Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11(9):633–643. doi:10.1038/nrm2957
Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10(11):778–790. doi:10.1038/nrm2786
Vicente-Manzanares M, Zareno J, Whitmore L, Choi CK, Horwitz AF (2007) Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J Cell Biol 176(5):573–580. doi:10.1083/jcb.200612043
Vicente-Manzanares M, Koach MA, Whitmore L, Lamers ML, Horwitz AF (2008) Segregation and activation of myosin IIB creates a rear in migrating cells. J Cell Biol 183(3):543–554. doi:10.1083/jcb.200806030
Zhang S, Wang G, Fernig DG, Rudland PS, Webb SE, Barraclough R, Martin-Fernandez M (2005) Interaction of metastasis-inducing S100A4 protein in vivo by fluorescence lifetime imaging microscopy. Eur Biophys J 34(1):19–27. doi:10.1007/s00249-004-0428-x
Ismail T, Fernig DG, Rudland PS, Terry CJ, Wang G, Barraclough R (2008) The basic C-terminal amino acids of calcium-binding protein S100A4 promote metastasis. Carcinogenesis 29(12):2259–2266. doi:10.1093/carcin/bgn217
Zhang S, Wang G, Liu D, Bao Z, Fernig DG, Rudland PS, Barraclough R (2005) The C-terminal region of S100A4 is important for its metastasis-inducing properties. Oncogene 24(27):4401–4411. doi:10.1038/sj.onc.1208663
Elliott PR, Irvine AF, Jung HS, Tozawa K, Pastok MW, Picone R, Badyal SK, Basran J, Rudland PS, Barraclough R, Lian LY, Bagshaw CR, Kriajevska M, Barsukov IL (2012) Asymmetric mode of Ca2+-S100A4 interaction with nonmuscle myosin IIA generates nanomolar affinity required for filament remodeling. Structure 20(4):654–666. doi:10.1016/j.str.2012.02.002
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(31):19679–19682
Hajra KM, Fearon ER (2002) Cadherin and catenin alterations in human cancer. Genes Chromosom Cancer 34(3):255–268. doi:10.1002/gcc.10083
Moriyama-Kita M, Endo Y, Yonemura Y, Heizmann CW, Miyamori H, Sato H, Yamamoto E, Sasaki T (2005) S100A4 regulates E-cadherin expression in oral squamous cell carcinoma. Cancer Lett 230(2):211–218. doi:10.1016/j.canlet.2004.12.046
Tubaro C, Arcuri C, Giambanco I, Donato R (2011) S100B in myoblasts regulates the transition from activation to quiescence and from quiescence to activation and reduces apoptosis. Biochim Biophys Acta 1813(5):1092–1104. doi:10.1016/j.bbamcr.2010.11.015
Brozzi F, Arcuri C, Giambanco I, Donato R (2009) S100B protein regulates astrocyte shape and migration via interaction with Src kinase: implications for astrocyte development, activation and tumour growth. J Biol Chem 284(13):8797–8811. doi:10.1074/jbc.M805897200
Sakaguchi M, Sonegawa H, Murata H, Kitazoe M, Futami J, Kataoka K, Yamada H, Huh NH (2008) S100A11, an dual mediator for growth regulation of human keratinocytes. Mol Biol Cell 19(1):78–85. doi:10.1091/mbc.E07-07-0682
Stein U, Arlt F, Walther W, Smith J, Waldman T, Harris ED, Mertins SD, Heizmann CW, Allard D, Birchmeier W, Schlag PM, Shoemaker RH (2006) The metastasis-associated gene S100A4 is a novel target of beta-catenin/T-cell factor signaling in colon cancer. Gastroenterology 131(5):1486–1500. doi:10.1053/j.gastro.2006.08.041
Stein U, Arlt F, Smith J, Sack U, Herrmann P, Walther W, Lemm M, Fichtner I, Shoemaker RH, Schlag PM (2011) Intervening in beta-catenin signaling by sulindac inhibits S100A4-dependent colon cancer metastasis. Neoplasia 13(2):131–144
Slomnicki LP, Lesniak W (2010) S100A6 (calcyclin) deficiency induces senescence-like changes in cell cycle, morphology and functional characteristics of mouse NIH 3T3 fibroblasts. J Cell Biochem 109(3):576–584. doi:10.1002/jcb.22434
Breen EC, Tang K (2003) Calcyclin (S100A6) regulates pulmonary fibroblast proliferation, morphology, and cytoskeletal organization in vitro. J Cell Biochem 88(4):848–854. doi:10.1002/jcb.10398
Luo X, Sharff KA, Chen J, He TC, Luu HH (2008) S100A6 expression and function in human osteosarcoma. Clin Orthop Relat Res 466(9):2060–2070. doi:10.1007/s11999-008-0361-x
Luu HH, Zhou L, Haydon RC, Deyrup AT, Montag AG, Huo D, Heck R, Heizmann CW, Peabody TD, Simon MA, He TC (2005) Increased expression of S100A6 is associated with decreased metastasis and inhibition of cell migration and anchorage independent growth in human osteosarcoma. Cancer Lett 229(1):135–148. doi:10.1016/j.canlet.2005.02.015
Nedjadi T, Kitteringham N, Campbell F, Jenkins RE, Park BK, Navarro P, Ashcroft F, Tepikin A, Neoptolemos JP, Costello E (2009) S100A6 binds to annexin 2 in pancreatic cancer cells and promotes pancreatic cancer cell motility. Br J Cancer 101(7):1145–1154. doi:10.1038/sj.bjc.6605289
Ohuchida K, Mizumoto K, Ishikawa N, Fujii K, Konomi H, Nagai E, Yamaguchi K, Tsuneyoshi M, Tanaka M (2005) The role of S100A6 in pancreatic cancer development and its clinical implication as a diagnostic marker and therapeutic target. Clin Cancer Res 11(21):7785–7793. doi:10.1158/1078-0432.CCR-05-0714
Lesniak W, Slomnicki LP, Filipek A (2009) S100A6—new facts and features. Biochem Biophys Res Commun 390(4):1087–1092. doi:10.1016/j.bbrc.2009.10.150
Komatsu K, Kobune-Fujiwara Y, Andoh A, Ishiguro S, Hunai H, Suzuki N, Kameyama M, Murata K, Miyoshi J, Akedo H, Tatsuta M, Nakamura H (2000) Increased expression of S100A6 at the invading fronts of the primary lesion and liver metastasis in patients with colorectal adenocarcinoma. Br J Cancer 83(6):769–774. doi:10.1054/bjoc.2000.1356
Guo XJ, Chambers AF, Parfett CL, Waterhouse P, Murphy LC, Reid RE, Craig AM, Edwards DR, Denhardt DT (1990) Identification of a serum-inducible messenger RNA (5B10) as the mouse homologue of calcyclin: tissue distribution and expression in metastatic, ras-transformed NIH 3T3 cells. Cell Growth Differ 1(7):333–338
Golitsina NL, Kordowska J, Wang CL, Lehrer SS (1996) Ca2+-dependent binding of calcyclin to muscle tropomyosin. Biochem Biophys Res Commun 220(2):360–365. doi:10.1006/bbrc.1996.0410
Gross SR (2013) Actin binding proteins: their ups and downs in metastatic life. Cell Adh Migr 7(2):199–213
Mani RS, Kay CM (1990) Isolation and characterization of a novel molecular weight 11,000 Ca2+-binding protein from smooth muscle. Biochemistry 29(6):1398–1404
Filipek A, Zasada A, Wojda U, Makuch R, Dabrowska R (1996) Characterization of chicken gizzard calcyclin and examination of its interaction with caldesmon. Comp Biochem Physiol B: Biochem Mol Biol 113(4):745–752
Wills FL, McCubbin WD, Kay CM (1994) Smooth muscle calponin-caltropin interaction: effect on biological activity and stability of calponin. Biochemistry 33(18):5562–5569
Wolf R, Howard OM, Dong HF, Voscopoulos C, Boeshans K, Winston J, Divi R, Gunsior M, Goldsmith P, Ahvazi B, Chavakis T, Oppenheim JJ, Yuspa SH (2008) Chemotactic activity of S100A7 (Psoriasin) is mediated by the receptor for advanced glycation end products and potentiates inflammation with highly homologous but functionally distinct S100A15. J Immunol 181(2):1499–1506
Nasser MW, Qamri Z, Deol YS, Ravi J, Powell CA, Trikha P, Schwendener RA, Bai XF, Shilo K, Zou X, Leone G, Wolf R, Yuspa SH, Ganju RK (2012) S100A7 enhances mammary tumorigenesis through upregulation of inflammatory pathways. Cancer Res 72(3):604–615. doi:10.1158/0008-5472.CAN-11-0669
Winston J, Wolf R (2012) Psoriasin (S100A7) promotes migration of a squamous carcinoma cell line. J Dermatol Sci 67(3):205–207. doi:10.1016/j.jdermsci.2012.06.009
Kataoka K, Ono T, Murata H, Morishita M, Yamamoto KI, Sakaguchi M, Huh NH (2012) S100A7 promotes the migration and invasion of osteosarcoma cells via the receptor for advanced glycation end products. Oncol Lett 3(5):1149–1153. doi:10.3892/ol.2012.612
Emberley ED, Niu Y, Leygue E, Tomes L, Gietz RD, Murphy LC, Watson PH (2003) Psoriasin interacts with Jab1 and influences breast cancer progression. Cancer Res 63(8):1954–1961
Morgan MR, Jazayeri M, Ramsay AG, Thomas GJ, Boulanger MJ, Hart IR, Marshall JF (2011) Psoriasin (S100A7) associates with integrin beta6 subunit and is required for alphavbeta6-dependent carcinoma cell invasion. Oncogene 30(12):1422–1435. doi:10.1038/onc.2010.535
West NR, Farnell B, Murray JI, Hof F, Watson PH, Boulanger MJ (2009) Structural and functional characterization of a triple mutant form of S100A7 defective for Jab1 binding. Protein Sci Publ Protein Soc 18(12):2615–2623. doi:10.1002/pro.274
West NR, Watson PH (2010) S100A7 (psoriasin) is induced by the proinflammatory cytokines oncostatin-M and interleukin-6 in human breast cancer. Oncogene 29(14):2083–2092. doi:10.1038/onc.2009.488
Pei XF, Noble MS, Davoli MA, Rosfjord E, Tilli MT, Furth PA, Russell R, Johnson MD, Dickson RB (2004) Explant-cell culture of primary mammary tumors from MMTV-c-Myc transgenic mice. In Vitro Cell Dev Biol Anim 40(1–2):14–21. doi:10.1290/1543-706X(2004)40<14:ECOPMT>2.0.CO;2
Deol YS, Nasser MW, Yu L, Zou X, Ganju RK (2011) Tumor-suppressive effects of psoriasin (S100A7) are mediated through the beta-catenin/T cell factor 4 protein pathway in estrogen receptor-positive breast cancer cells. J Biol Chem 286(52):44845–44854. doi:10.1074/jbc.M111.225466
Krop I, Marz A, Carlsson H, Li X, Bloushtain-Qimron N, Hu M, Gelman R, Sabel MS, Schnitt S, Ramaswamy S, Kleer CG, Enerback C, Polyak K (2005) A putative role for psoriasin in breast tumor progression. Cancer Res 65(24):11326–11334. doi:10.1158/0008-5472.CAN-05-1523
Goyette J, Geczy CL (2011) Inflammation-associated S100 proteins: new mechanisms that regulate function. Amino Acids 41(4):821–842. doi:10.1007/s00726-010-0528-0
Ryckman C, Vandal K, Rouleau P, Talbot M, Tessier PA (2003) Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J Immunol 170(6):3233–3242
Frosch M, Strey A, Vogl T, Wulffraat NM, Kuis W, Sunderkotter C, Harms E, Sorg C, Roth J (2000) Myeloid-related proteins 8 and 14 are specifically secreted during interaction of phagocytes and activated endothelium and are useful markers for monitoring disease activity in pauciarticular-onset juvenile rheumatoid arthritis. Arthritis Rheum 43(3):628–637. doi:10.1002/1529-0131(200003)43:3<628:AID-ANR20>3.0.CO;2-X
Odink K, Cerletti N, Bruggen J, Clerc RG, Tarcsay L, Zwadlo G, Gerhards G, Schlegel R, Sorg C (1987) Two calcium-binding proteins in infiltrate macrophages of rheumatoid arthritis. Nature 330(6143):80–82. doi:10.1038/330080a0
Zwadlo G, Bruggen J, Gerhards G, Schlegel R, Sorg C (1988) Two calcium-binding proteins associated with specific stages of myeloid cell differentiation are expressed by subsets of macrophages in inflammatory tissues. Clin Exp Immunol 72(3):510–515
Foell D, Frosch M, Sorg C, Roth J (2004) Phagocyte-specific calcium-binding S100 proteins as clinical laboratory markers of inflammation. Clin Chim Acta 344(1–2):37–51. doi:10.1016/j.cccn.2004.02.023
Li C, Li S, Jia C, Yang L, Song Z, Wang Y (2012) Low concentration of S100A8/9 promotes angiogenesis-related activity of vascular endothelial cells: bridges among inflammation, angiogenesis, and tumorigenesis? Mediat Inflamm 2012:248574. doi:10.1155/2012/248574
Lee Y, Jang S, Min JK, Lee K, Sohn KC, Lim JS, Im M, Lee HE, Seo YJ, Kim CD, Lee JH (2012) S100A8 and S100A9 are messengers in the crosstalk between epidermis and dermis modulating a psoriatic milieu in human skin. Biochem Biophys Res Commun 423(4):647–653. doi:10.1016/j.bbrc.2012.05.162
Hermani A, De Servi B, Medunjanin S, Tessier PA, Mayer D (2006) S100A8 and S100A9 activate MAP kinase and NF-kappaB signaling pathways and trigger translocation of RAGE in human prostate cancer cells. Exp Cell Res 312(2):184–197. doi:10.1016/j.yexcr.2005.10.013
Ang CW, Nedjadi T, Sheikh AA, Tweedle EM, Tonack S, Honap S, Jenkins RE, Park BK, Schwarte-Waldhoff I, Khattak I, Azadeh B, Dodson A, Kalirai H, Neoptolemos JP, Rooney PS, Costello E (2010) Smad4 loss is associated with fewer S100A8-positive monocytes in colorectal tumors and attenuated response to S100A8 in colorectal and pancreatic cancer cells. Carcinogenesis 31(9):1541–1551. doi:10.1093/carcin/bgq137
Ichikawa M, Williams R, Wang L, Vogl T, Srikrishna G (2011) S100A8/A9 activate key genes and pathways in colon tumor progression. Mol Cancer Res MCR 9(2):133–148. doi:10.1158/1541-7786.MCR-10-0394
Saha A, Lee YC, Zhang Z, Chandra G, Su SB, Mukherjee AB (2010) Lack of an endogenous anti-inflammatory protein in mice enhances colonization of B16F10 melanoma cells in the lungs. J Biol Chem 285(14):10822–10831. doi:10.1074/jbc.M109.083550
Newton RA, Hogg N (1998) The human S100 protein MRP-14 is a novel activator of the beta 2 integrin Mac-1 on neutrophils. J Immunol 160(3):1427–1435
Hibino T, Sakaguchi M, Miyamoto S, Yamamoto M, Motoyama A, Hosoi J, Shimokata T, Ito T, Tsuboi R, Huh NH (2013) S100A9 Is a novel ligand of EMMPRIN that promotes melanoma metastasis. Cancer Res 73(1):172–183. doi:10.1158/0008-5472.CAN-11-3843
Cornish CJ, Devery JM, Poronnik P, Lackmann M, Cook DI, Geczy CL (1996) S100 protein CP-10 stimulates myeloid cell chemotaxis without activation. J Cell Physiol 166(2):427–437. doi:10.1002/(SICI)1097-4652(199602)166:2<427:AID-JCP21>3.0.CO;2-6
Hiratsuka S, Watanabe A, Aburatani H, Maru Y (2006) Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol 8(12):1369–1375. doi:10.1038/ncb1507
Lominadze G, Rane MJ, Merchant M, Cai J, Ward RA, McLeish KR (2005) Myeloid-related protein-14 is a p38 MAPK substrate in human neutrophils. J Immunol 174(11):7257–7267
Manitz MP, Horst B, Seeliger S, Strey A, Skryabin BV, Gunzer M, Frings W, Schonlau F, Roth J, Sorg C, Nacken W (2003) Loss of S100A9 (MRP14) results in reduced interleukin-8-induced CD11b surface expression, a polarized microfilament system, and diminished responsiveness to chemoattractants in vitro. Mol Cell Biol 23(3):1034–1043
Vogl T, Ludwig S, Goebeler M, Strey A, Thorey IS, Reichelt R, Foell D, Gerke V, Manitz MP, Nacken W, Werner S, Sorg C, Roth J (2004) MRP8 and MRP14 control microtubule reorganization during transendothelial migration of phagocytes. Blood 104(13):4260–4268. doi:10.1182/blood-2004-02-0446
Roth J, Burwinkel F, van den Bos C, Goebeler M, Vollmer E, Sorg C (1993) MRP8 and MRP14, S-100-like proteins associated with myeloid differentiation, are translocated to plasma membrane and intermediate filaments in a calcium-dependent manner. Blood 82(6):1875–1883
Leukert N, Vogl T, Strupat K, Reichelt R, Sorg C, Roth J (2006) Calcium-dependent tetramer formation of S100A8 and S100A9 is essential for biological activity. J Mol Biol 359(4):961–972. doi:10.1016/j.jmb.2006.04.009
McNeill E, Conway SJ, Roderick HL, Bootman MD, Hogg N (2007) Defective chemoattractant-induced calcium signalling in S100A9 null neutrophils. Cell Calcium 41(2):107–121. doi:10.1016/j.ceca.2006.05.004
Vandal K, Rouleau P, Boivin A, Ryckman C, Talbot M, Tessier PA (2003) Blockade of S100A8 and S100A9 suppresses neutrophil migration in response to lipopolysaccharide. J Immunol 171(5):2602–2609
O’Connell PA, Surette AP, Liwski RS, Svenningsson P, Waisman DM (2010) S100A10 regulates plasminogen-dependent macrophage invasion. Blood 116(7):1136–1146. doi:10.1182/blood-2010-01-264754
Phipps KD, Surette AP, O’Connell PA, Waisman DM (2011) Plasminogen receptor S100A10 is essential for the migration of tumor-promoting macrophages into tumor sites. Cancer Res 71(21):6676–6683. doi:10.1158/0008-5472.CAN-11-1748
McKiernan E, McDermott EW, Evoy D, Crown J, Duffy MJ (2011) The role of S100 genes in breast cancer progression. Tumour Biol J Int Soc Oncodev Biol Med 32(3):441–450. doi:10.1007/s13277-010-0137-2
Zhang L, Fogg DK, Waisman DM (2004) RNA interference-mediated silencing of the S100A10 gene attenuates plasmin generation and invasiveness of Colo 222 colorectal cancer cells. J Biol Chem 279(3):2053–2062. doi:10.1074/jbc.M310357200
Choi KS, Fogg DK, Yoon CS, Waisman DM (2003) p11 regulates extracellular plasmin production and invasiveness of HT1080 fibrosarcoma cells. FASEB J Off Publ Fed Am Soc Exp Biol 17(2):235–246. doi:10.1096/fj.02-0697com
Jung MJ, Murzik U, Wehder L, Hemmerich P, Melle C (2010) Regulation of cellular actin architecture by S100A10. Exp Cell Res 316(7):1234–1240. doi:10.1016/j.yexcr.2010.01.022
Yang X, Popescu NC, Zimonjic DB (2011) DLC1 interaction with S100A10 mediates inhibition of in vitro cell invasion and tumorigenicity of lung cancer cells through a RhoGAP-independent mechanism. Cancer Res 71(8):2916–2925. doi:10.1158/0008-5472.CAN-10-2158
Zobiack N, Gerke V, Rescher U (2001) Complex formation and submembranous localization of annexin 2 and S100A10 in live HepG2 cells. FEBS Lett 500(3):137–140
Gerke V, Weber K (1984) Identity of p36K phosphorylated upon Rous sarcoma virus transformation with a protein purified from brush borders; calcium-dependent binding to non-erythroid spectrin and F-actin. EMBO J 3(1):227–233
Glenney JR Jr (1987) Calpactins: calcium-regulated membrane-skeletal proteins. BioEssays 7(4):173–175. doi:10.1002/bies.950070408
Regnouf F, Rendon A, Pradel LA (1991) Biochemical characterization of annexins I and II isolated from pig nervous tissue. J Neurochem 56(6):1985–1996
Murzik U, Hemmerich P, Weidtkamp-Peters S, Ulbricht T, Bussen W, Hentschel J, von Eggeling F, Melle C (2008) Rad54B targeting to DNA double-strand break repair sites requires complex formation with S100A11. Mol Biol Cell 19(7):2926–2935. doi:10.1091/mbc.E07-11-1167
Sakaguchi M, Miyazaki M, Inoue Y, Tsuji T, Kouchi H, Tanaka T, Yamada H, Namba M (2000) Relationship between contact inhibition and intranuclear S100C of normal human fibroblasts. J Cell Biol 149(6):1193–1206
Sakaguchi M, Huh NH (2011) S100A11, a dual growth regulator of epidermal keratinocytes. Amino Acids 41(4):797–807. doi:10.1007/s00726-010-0747-4
Fan C, Fu Z, Su Q, Angelini DJ, Van Eyk J, Johns RA (2011) S100A11 mediates hypoxia-induced mitogenic factor (HIMF)-induced smooth muscle cell migration, vesicular exocytosis, and nuclear activation. Mol Cell Proteomics 10(3):M110000901. doi:10.1074/mcp.M110.000901
Naka M, Qing ZX, Sasaki T, Kise H, Tawara I, Hamaguchi S, Tanaka T (1994) Purification and characterization of a novel calcium-binding protein, S100C, from porcine heart. Biochim Biophys Acta 1223(3):348–353
Vogl T, Propper C, Hartmann M, Strey A, Strupat K, van den Bos C, Sorg C, Roth J (1999) S100A12 is expressed exclusively by granulocytes and acts independently from MRP8 and MRP14. J Biol Chem 274(36):25291–25296
Guignard F, Mauel J, Markert M (1995) Identification and characterization of a novel human neutrophil protein related to the S100 family. Biochem J 309(2):395–401
Yang Z, Tao T, Raftery MJ, Youssef P, Di Girolamo N, Geczy CL (2001) Proinflammatory properties of the human S100 protein S100A12. J Leukoc Biol 69(6):986–994
Dell’Angelica EC, Schleicher CH, Santome JA (1994) Primary structure and binding properties of calgranulin C, a novel S100-like calcium-binding protein from pig granulocytes. J Biol Chem 269(46):28929–28936
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(7):889–901
Yan WX, Armishaw C, Goyette J, Yang Z, Cai H, Alewood P, Geczy CL (2008) Mast cell and monocyte recruitment by S100A12 and its hinge domain. J Biol Chem 283(19):13035–13043. doi:10.1074/jbc.M710388200
Rouleau P, Vandal K, Ryckman C, Poubelle PE, Boivin A, Talbot M, Tessier PA (2003) The calcium-binding protein S100A12 induces neutrophil adhesion, migration, and release from bone marrow in mouse at concentrations similar to those found in human inflammatory arthritis. Clin Immunol 107(1):46–54
Xiong Z, O’Hanlon D, Becker LE, Roder J, MacDonald JF, Marks A (2000) Enhanced calcium transients in glial cells in neonatal cerebellar cultures derived from S100B null mice. Exp Cell Res 257(2):281–289. doi:10.1006/excr.2000.4902
Lin J, Yang Q, Wilder PT, Carrier F, Weber DJ (2010) The calcium-binding protein S100B down-regulates p53 and apoptosis in malignant melanoma. J Biol Chem 285(35):27487–27498. doi:10.1074/jbc.M110.155382
Leclerc E, Fritz G, Weibel M, Heizmann CW, Galichet A (2007) S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains. J Biol Chem 282(43):31317–31331. doi:10.1074/jbc.M703951200
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(51):40096–40105. doi:10.1074/jbc.M006993200
Bianchi R, Kastrisianaki E, Giambanco I, Donato R (2011) S100B protein stimulates microglia migration via RAGE-dependent up-regulation of chemokine expression and release. J Biol Chem 286(9):7214–7226. doi:10.1074/jbc.M110.169342
Reddy MA, Li SL, Sahar S, Kim YS, Xu ZG, Lanting L, Natarajan R (2006) Key role of Src kinase in S100B-induced activation of the receptor for advanced glycation end products in vascular smooth muscle cells. J Biol Chem 281(19):13685–13693. doi:10.1074/jbc.M511425200
Sbai O, Devi TS, Melone MA, Feron F, Khrestchatisky M, Singh LP, Perrone L (2010) RAGE-TXNIP axis is required for S100B-promoted Schwann cell migration, fibronectin expression and cytokine secretion. J Cell Sci 123(24):4332–4339. doi:10.1242/jcs.074674
Pang X, Min J, Liu L, Liu Y, Ma N, Zhang H (2012) S100B protein as a possible participant in the brain metastasis of NSCLC. Med Oncol 29(4):2626–2632. doi:10.1007/s12032-012-0169-0
Jiang W, Jia Q, Liu L, Zhao X, Tan A, Ma N, Zhang H (2011) S100B promotes the proliferation, migration and invasion of specific brain metastatic lung adenocarcinoma cell line. Cell Biochem Funct 29(7):582–588. doi:10.1002/cbf.1791
Ivanenkov VV, Jamieson GA, Jr., Gruenstein E, Dimlich RV (1995) Characterization of S-100b binding epitopes. Identification of a novel target, the actin capping protein, CapZ. J Biol Chem 270(24):14651–14658
Skripnikova EV, Gusev NB (1989) Interaction of smooth muscle caldesmon with S-100 protein. FEBS Lett 257(2):380–382
Donato R (1988) Calcium-independent, pH-regulated effects of S-100 proteins on assembly-disassembly of brain microtubule protein in vitro. J Biol Chem 263(1):106–110
Baudier J, Cole RD (1988) Interactions between the microtubule-associated tau proteins and S100b regulate tau phosphorylation by the Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 263(12):5876–5883
Sorci G, Agneletti AL, Bianchi R, Donato R (1998) Association of S100B with intermediate filaments and microtubules in glial cells. Biochim Biophys Acta 1448(2):277–289
Saito T, Ikeda T, Nakamura K, Chung UI, Kawaguchi H (2007) S100A1 and S100B, transcriptional targets of SOX trio, inhibit terminal differentiation of chondrocytes. EMBO Rep 8(5):504–509. doi:10.1038/sj.embor.7400934
Wang G, Platt-Higgins A, Carroll J, de Silva Rudland S, Winstanley J, Barraclough R, Rudland PS (2006) Induction of metastasis by S100P in a rat mammary model and its association with poor survival of breast cancer patients. Cancer Res 66(2):1199–1207. doi:10.1158/0008-5472.CAN-05-2605
Guerreiro Da Silva ID, Hu YF, Russo IH, Ao X, Salicioni AM, Yang X, Russo J (2000) S100P calcium-binding protein overexpression is associated with immortalization of human breast epithelial cells in vitro and early stages of breast cancer development in vivo. Int J Oncol 16(2):231–240
Gibadulinova A, Tothova V, Pastorek J, Pastorekova S (2011) Transcriptional regulation and functional implication of S100P in cancer. Amino Acids 41(4):885–892. doi:10.1007/s00726-010-0495-5
Parkkila S, Pan PW, Ward A, Gibadulinova A, Oveckova I, Pastorekova S, Pastorek J, Martinez AR, Helin HO, Isola J (2008) The calcium-binding protein S100P in normal and malignant human tissues. BMC Clin Pathol 8:2. doi:10.1186/1472-6890-8-2
Tong XM, Lin XN, Song T, Liu L, Zhang SY (2010) Calcium-binding protein S100P is highly expressed during the implantation window in human endometrium. Fertil Steril 94(4):1510–1518. doi:10.1016/j.fertnstert.2009.07.1667
Arumugam T, Logsdon CD (2011) S100P: a novel therapeutic target for cancer. Amino Acids 41(4):893–899. doi:10.1007/s00726-010-0496-4
Du M, Wang G, Ismail TM, Gross S, Fernig DG, Barraclough R, Rudland PS (2012) S100P dissociates myosin IIA filaments and focal adhesion sites to reduce cell adhesion and enhance cell migration. J Biol Chem 287(19):15330–15344. doi:10.1074/jbc.M112.349787
Austermann J, Nazmi AR, Muller-Tidow C, Gerke V (2008) Characterization of the Ca2+-regulated ezrin-S100P interaction and its role in tumor cell migration. J Biol Chem 283(43):29331–29340. doi:10.1074/jbc.M806145200
Arumugam T, Simeone DM, Van Golen K, Logsdon CD (2005) S100P promotes pancreatic cancer growth, survival, and invasion. Clin Cancer Res 11(15):5356–5364. doi:10.1158/1078-0432.CCR-05-0092
Zhou C, Zhong Q, Rhodes LV, Townley I, Bratton MR, Zhang Q, Martin EC, Elliott S, Collins-Burow BM, Burow ME, Wang G (2012) Proteomic analysis of acquired tamoxifen resistance in MCF-7 cells reveals expression signatures associated with enhanced migration. Breast Cancer Res BCR 14(2):R45. doi:10.1186/bcr3144
Jiang L, Lai YK, Zhang J, Wang H, Lin MC, He ML, Kung HF (2011) Targeting S100P inhibits colon cancer growth and metastasis by Lentivirus-mediated RNA interference and proteomic analysis. Mol Med 17(7–8):709–716. doi:10.2119/molmed.2011.00008
Chandramouli A, Mercado-Pimentel ME, Hutchinson A, Gibadulinova A, Olson ER, Dickinson S, Shanas R, Davenport J, Owens J, Bhattacharyya AK, Regan JW, Pastorekova S, Arumugam T, Logsdon CD, Nelson MA (2010) The induction of S100p expression by the prostaglandin E(2) (PGE(2))/EP4 receptor signaling pathway in colon cancer cells. Cancer Biol Ther 10(10):1056–1066. doi:10.4161/cbt.10.10.13373
Barry S, Chelala C, Lines K, Sunamura M, Wang A, Marelli-Berg FM, Brennan C, Lemoine NR, Crnogorac-Jurcevic T (2012) S100P is a metastasis-associated gene that facilitates transendothelial migration of pancreatic cancer cells. Clin Exp Metastasis 30(3):251–264. doi:10.1007/s10585-012-9532-y
Heil A, Nazmi AR, Koltzscher M, Poeter M, Austermann J, Assard N, Baudier J, Kaibuchi K, Gerke V (2011) S100P is a novel interaction partner and regulator of IQGAP1. J Biol Chem 286(9):7227–7238. doi:10.1074/jbc.M110.135095
Whiteman HJ, Weeks ME, Dowen SE, Barry S, Timms JF, Lemoine NR, Crnogorac-Jurcevic T (2007) The role of S100P in the invasion of pancreatic cancer cells is mediated through cytoskeletal changes and regulation of cathepsin D. Cancer Res 67(18):8633–8642. doi:10.1158/0008-5472.CAN-07-0545
Fuentes MK, Nigavekar SS, Arumugam T, Logsdon CD, Schmidt AM, Park JC, Huang EH (2007) RAGE activation by S100P in colon cancer stimulates growth, migration, and cell signaling pathways. Dis Colon Rectum 50(8):1230–1240. doi:10.1007/s10350-006-0850-5
Halayko AJ, Ghavami S (2009) S100A8/A9: a mediator of severe asthma pathogenesis and morbidity? Can J Physiol Pharmacol 87(10):743–755. doi:10.1139/Y09-054
Michetti F, Corvino V, Geloso MC, Lattanzi W, Bernardini C, Serpero L, Gazzolo D (2012) The S100B protein in biological fluids: more than a lifelong biomarker of brain distress. J Neurochem 120(5):644–659. doi:10.1111/j.1471-4159.2011.07612.x
Wolf R, Ruzicka T, Yuspa SH (2011) Novel S100A7 (psoriasin)/S100A15 (koebnerisin) subfamily: highly homologous but distinct in regulation and function. Amino Acids 41(4):789–796. doi:10.1007/s00726-010-0666-4
Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ, Geczy CL (2013) Functions of S100 proteins. Curr Mol Med 13(1):24–57
Yoo HJ, Yun BR, Kwon JH, Ahn HS, Seol MA, Lee MJ, Yu GR, Yu HC, Hong B, Choi K, Kim DG (2009) Genetic and expression alterations in association with the sarcomatous change of cholangiocarcinoma cells. Exp Mol Med 41(2):102–115
Hamada S, Satoh K, Hirota M, Fujibuchi W, Kanno A, Umino J, Ito H, Satoh A, Kikuta K, Kume K, Masamune A, Shimosegawa T (2009) Expression of the calcium-binding protein S100P is regulated by bone morphogenetic protein in pancreatic duct epithelial cell lines. Cancer Sci 100(1):103–110. doi:10.1111/j.1349-7006.2008.00993.x
Psaila B, Lyden D (2009) The metastatic niche: adapting the foreign soil. Nat Rev Cancer 9(4):285–293. doi:10.1038/nrc2621
Grum-Schwensen B, Klingelhofer J, Berg CH, El-Naaman C, Grigorian M, Lukanidin E, Ambartsumian N (2005) Suppression of tumor development and metastasis formation in mice lacking the S100A4(mts1) gene. Cancer Res 65(9):3772–3780. doi:10.1158/0008-5472.CAN-04-4510
Schmidt-Hansen B, Klingelhofer J, Grum-Schwensen B, Christensen A, Andresen S, Kruse C, Hansen T, Ambartsumian N, Lukanidin E, Grigorian M (2004) Functional significance of metastasis-inducing S100A4(Mts1) in tumor-stroma interplay. J Biol Chem 279(23):24498–24504. doi:10.1074/jbc.M400441200
Grum-Schwensen B, Klingelhofer J, Grigorian M, Almholt K, Nielsen BS, Lukanidin E, Ambartsumian N (2010) Lung metastasis fails in MMTV-PyMT oncomice lacking S100A4 due to a T-cell deficiency in primary tumors. Cancer Res 70(3):936–947. doi:10.1158/0008-5472.CAN-09-3220
Taylor S, Herrington S, Prime W, Rudland PS, Barraclough R (2002) S100A4 (p9Ka) protein in colon carcinoma and liver metastases: association with carcinoma cells and T-lymphocytes. Br J Cancer 86(3):409–416. doi:10.1038/sj.bjc.6600071
Ruegg C (2006) Leukocytes, inflammation, and angiogenesis in cancer: fatal attractions. J Leukoc Biol 80(4):682–684. doi:10.1189/jlb.0606394
Salama I, Malone PS, Mihaimeed F, Jones JL (2008) A review of the S100 proteins in cancer. Eur J Surg Oncol 34(4):357–364. doi:10.1016/j.ejso.2007.04.009
Guarino M, Tosoni A, Nebuloni M (2009) Direct contribution of epithelium to organ fibrosis: epithelial–mesenchymal transition. Hum Pathol 40(10):1365–1376. doi:10.1016/j.humpath.2009.02.020
Rygiel KA, Robertson H, Marshall HL, Pekalski M, Zhao L, Booth TA, Jones DE, Burt AD, Kirby JA (2008) Epithelial–mesenchymal transition contributes to portal tract fibrogenesis during human chronic liver disease. Lab Investig J Tech Meth Pathol 88(2):112–123. doi:10.1038/labinvest.3700704
Ju W, Eichinger F, Bitzer M, Oh J, McWeeney S, Berthier CC, Shedden K, Cohen CD, Henger A, Krick S, Kopp JB, Stoeckert CJ Jr, Dikman S, Schroppel B, Thomas DB, Schlondorff D, Kretzler M, Bottinger EP (2009) Renal gene and protein expression signatures for prediction of kidney disease progression. Am J Pathol 174(6):2073–2085. doi:10.2353/ajpath.2009.080888
Gant TW, Baus PR, Clothier B, Riley J, Davies R, Judah DJ, Edwards RE, George E, Greaves P, Smith AG (2003) Gene expression profiles associated with inflammation, fibrosis, and cholestasis in mouse liver after griseofulvin. EHP Toxicogenomics J Natl Inst Environ Health Sci 111(1T):37–43
Dempsie Y, Nilsen M, White K, Mair KM, Loughlin L, Ambartsumian N, Rabinovitch M, Maclean MR (2011) Development of pulmonary arterial hypertension in mice over-expressing S100A4/Mts1 is specific to females. Respir Res 12:159. doi:10.1186/1465-9921-12-159
Merklinger SL, Wagner RA, Spiekerkoetter E, Hinek A, Knutsen RH, Kabir MG, Desai K, Hacker S, Wang L, Cann GM, Ambartsumian NS, Lukanidin E, Bernstein D, Husain M, Mecham RP, Starcher B, Yanagisawa H, Rabinovitch M (2005) Increased fibulin-5 and elastin in S100A4/Mts1 mice with pulmonary hypertension. Circ Res 97(6):596–604. doi:10.1161/01.RES.0000182425.49768.8a
Schneider M, Kostin S, Strom CC, Aplin M, Lyngbaek S, Theilade J, Grigorian M, Andersen CB, Lukanidin E, Lerche Hansen J, Sheikh SP (2007) S100A4 is upregulated in injured myocardium and promotes growth and survival of cardiac myocytes. Cardiovasc Res 75(1):40–50. doi:10.1016/j.cardiores.2007.03.027
Kraus C, Rohde D, Weidenhammer C, Qiu G, Pleger ST, Voelkers M, Boerries M, Remppis A, Katus HA, Most P (2009) S100A1 in cardiovascular health and disease: closing the gap between basic science and clinical therapy. J Mol Cell Cardiol 47(4):445–455. doi:10.1016/j.yjmcc.2009.06.003
Yammani RR (2012) S100 proteins in cartilage: role in arthritis. Biochim Biophys Acta 1822(4):600–606. doi:10.1016/j.bbadis.2012.01.006
Bian L, Strzyz P, Jonsson IM, Erlandsson M, Hellvard A, Brisslert M, Ohlsson C, Ambartsumian N, Grigorian M, Bokarewa M (2011) S100A4 deficiency is associated with efficient bacterial clearance and protects against joint destruction during Staphylococcal infection. J Infect Dis 204(5):722–730. doi:10.1093/infdis/jir369
Heo SH, Choi YJ, Lee JH, Lee JM, Cho JY (2011) S100A2 level changes are related to human periodontitis. Mol Cells 32(5):445–450. doi:10.1007/s10059-011-0132-5
Madsen P, Rasmussen HH, Leffers H, Honore B, Dejgaard K, Olsen E, Kiil J, Walbum E, Andersen AH, Basse B et al (1991) Molecular cloning, occurrence, and expression of a novel partially secreted protein “psoriasin” that is highly up-regulated in psoriatic skin. J Invest Dermatol 97(4):701–712
Wolk K, Witte E, Wallace E, Docke WD, Kunz S, Asadullah K, Volk HD, Sterry W, Sabat R (2006) IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: a potential role in psoriasis. Eur J Immunol 36(5):1309–1323. doi:10.1002/eji.200535503
Glaser R, Harder J, Lange H, Bartels J, Christophers E, Schroder JM (2005) Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 6(1):57–64. doi:10.1038/ni1142
Gebhardt C, Nemeth J, Angel P, Hess J (2006) S100A8 and S100A9 in inflammation and cancer. Biochem Pharmacol 72(11):1622–1631. doi:10.1016/j.bcp.2006.05.017
Yano J, Noverr MC, Fidel PL Jr (2012) Cytokines in the host response to Candida vaginitis: identifying a role for non-classical immune mediators, S100 alarmins. Cytokine 58(1):118–128. doi:10.1016/j.cyto.2011.11.021
Rudland PS, Barraclough R, Fernig DG, Smith JA (1996) Mammary stem cells in normal development and cancer. In: Stem cells. Academic Press, London
Rudland PS, Paterson FC, Monaghan P, Davies AC, Warburton MJ (1986) Isolation and properties of rat cell lines morphologically intermediate between cultured mammary epithelial and myoepithelial-like cells. Dev Biol 113(2):388–405
Jamieson S, Rudland PS (1990) Identification of metaplastic variants generated by transfection of a nonmetastatic rat mammary epithelial cell line with DNA from a metastatic rat mammary cell line. Am J Pathol 137(3):629–641
Rudland PS, Wang G (2013) MicroRNAs in S100P-induced breast cancer metastasis. Cancer and Polio Research Fund UK annual report
Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10(5):593–601. doi:10.1038/ncb1722
Wang Z, Griffin M (2013) The role of TG2 in regulating S100A4-mediated mammary tumour cell migration. PLoS ONE 8(3):e57017. doi:10.1371/journal.pone.0057017
Rudland PS, Wang G (2013b) Role of microtubules in S100P-induced cell migration and metastasis. Cancer and Polio Research Fund UK annual report
Zhang H, Wang G, Ding Y, Wang Z, Barraclough R, Rudland PS, Fernig DG, Rao Z (2003) The crystal structure at 2A resolution of the Ca2+-binding protein S100P. J Mol Biol 325(4):785–794
Wang G, Rudland PS, White MR, Barraclough R (2000) Interaction in vivo and in vitro of the metastasis-inducing S100 protein, S100A4 (p9Ka) with S100A1. J Biol Chem 275(15):11141–11146
Wang G, Zhang S, Fernig DG, Spiller D, Martin-Fernandez M, Zhang H, Ding Y, Rao Z, Rudland PS, Barraclough R (2004) Heterodimeric interaction and interfaces of S100A1 and S100P. Biochem J 382(1):375–383. doi:10.1042/BJ20040142
Rudland PS, Fernig DG, Barraclough R (2013c) Identification of assays and potential inhibitors for metastasis-inducing proteins. Cancer and Polio Research Fund UK annual report
Barraclough R, Fernig DG, Rudland PS, Smith JA (1990) Synthesis of basic fibroblast growth factor upon differentiation of rat mammary epithelial to myoepithelial-like cells in culture. J Cell Physiol 144(2):333–344. doi:10.1002/jcp.1041440220
Rudland PS, Platt-Higgins AM, Wilkinson MC, Fernig DG (1993) Immunocytochemical identification of basic fibroblast growth factor in the developing rat mammary gland: variations in location are dependent on glandular structure and differentiation. J Histochem Cytochem 41(6):887–898
Duchesne L, Octeau V, Bearon RN, Beckett A, Prior IA, Lounis B, Fernig DG (2012) Transport of fibroblast growth factor 2 in the pericellular matrix is controlled by the spatial distribution of its binding sites in heparan sulfate. PLoS Biol 10(7):e1001361. doi:10.1371/journal.pbio.1001361
Barraclough R, Ismail T (2009) Effect of S100A4 on the establishment/development of metastases. Cancer and Polio Research Fund UK annual report
Ismail TM, Zhang S, Fernig DG, Gross S, Martin-Fernandez ML, See V, Tozawa K, Tynan CJ, Wang G, Wilkinson MC, Rudland PS, Barraclough R (2010) Self-association of calcium-binding protein S100A4 and metastasis. J Biol Chem 285(2):914–922. doi:10.1074/jbc.M109.010892
Ramasamy R, Yan SF, Schmidt AM (2011) Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann N Y Acad Sci 1243:88–102. doi:10.1111/j.1749-6632.2011.06320.x
Most P, Raake P, Weber C, Katus HA, Pleger ST (2013) S100A1 gene therapy in small and large animals. Methods Mol Biol 963:407–420. doi:10.1007/978-1-62703-230-8_25
Sack U, Walther W, Scudiero D, Selby M, Kobelt D, Lemm M, Fichtner I, Schlag PM, Shoemaker RH, Stein U (2011) Novel effect of antihelminthic Niclosamide on S100A4-mediated metastatic progression in colon cancer. J Natl Cancer Inst 103(13):1018–1036. doi:10.1093/jnci/djr190
Lapi E, Iovino A, Fontemaggi G, Soliera AR, Lacovelli S, Sacchi A, Rechavi G, Givol D, Blandino G, Strano S (2006) S100A2 gene is a direct transcriptional target of p53 homologues during keratinocyte differentiation. Oncogene 25(26):3628–3637. doi:10.1038/sj.onc.1209401
Shi Y, Zou M, Collison K, Baitei EY, Al-Makhalafi Z, Farid NR, Al-Mohanna FA (2006) Ribonucleic acid interference targeting S100A4 (Mts1) suppresses tumor growth and metastasis of anaplastic thyroid carcinoma in a mouse model. J Clin Endocrinol Metab 91(6):2373–2379. doi:10.1210/jc.2006-0155
Tamaki Y, Iwanaga Y, Niizuma S, Kawashima T, Kato T, Inuzuka Y, Horie T, Morooka H, Takase T, Akahashi Y, Kobuke K, Ono K, Shioi T, Sheikh SP, Ambartsumian N, Lukanidin E, Koshimizu TA, Miyazaki S, Kimura T (2013) Metastasis-associated protein, S100A4 mediates cardiac fibrosis potentially through the modulation of p53 in cardiac fibroblasts. J Mol Cell Cardiol 57:72–81. doi:10.1016/j.yjmcc.2013.01.007
Stary M, Schneider M, Sheikh SP, Weitzer G (2006) Parietal endoderm secreted S100A4 promotes early cardiomyogenesis in embryoid bodies. Biochem Biophys Res Commun 343(2):555–563. doi:10.1016/j.bbrc.2006.02.161
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(52):41278–41286. doi:10.1074/jbc.M007058200
Kiryushko D, Novitskaya V, Soroka V, Klingelhofer J, Lukanidin E, Berezin V, Bock E (2006) Molecular mechanisms of Ca2+ signaling in neurons induced by the S100A4 protein. Mol Cell Biol 26(9):3625–3638. doi:10.1128/MCB.26.9.3625-3638.2006
Hwang R, Lee EJ, Kim MH, Li SZ, Jin YJ, Rhee Y, Kim YM, Lim SK (2004) Calcyclin, a Ca2+ ion-binding protein, contributes to the anabolic effects of simvastatin on bone. J Biol Chem 279(20):21239–21247. doi:10.1074/jbc.M312771200
Shubbar E, Vegfors J, Carlstrom M, Petersson S, Enerback C (2012) Psoriasin (S100A7) increases the expression of ROS and VEGF and acts through RAGE to promote endothelial cell proliferation. Breast Cancer Res Treat 134(1):71–80. doi:10.1007/s10549-011-1920-5
Zhou G, Xie TX, Zhao M, Jasser SA, Younes MN, Sano D, Lin J, Kupferman ME, Santillan AA, Patel V, Gutkind JS, Ei-Naggar AK, Emberley ED, Watson PH, Matsuzawa SI, Reed JC, Myers JN (2008) Reciprocal negative regulation between S100A7/psoriasin and beta-catenin signaling plays an important role in tumor progression of squamous cell carcinoma of oral cavity. Oncogene 27(25):3527–3538. doi:10.1038/sj.onc.1211015
Vegfors J, Petersson S, Kovacs A, Polyak K, Enerback C (2012) The expression of Psoriasin (S100A7) and CD24 is linked and related to the differentiation of mammary epithelial cells. PLoS ONE 7(12):e53119. doi:10.1371/journal.pone.0053119
Voss A, Bode G, Sopalla C, Benedyk M, Varga G, Bohm M, Nacken W, Kerkhoff C (2011) Expression of S100A8/A9 in HaCaT keratinocytes alters the rate of cell proliferation and differentiation. FEBS Lett 585(2):440–446. doi:10.1016/j.febslet.2010.12.037
Ito Y, Arai K, Nozawa R, Yoshida H, Hirokawa M, Fukushima M, Inoue H, Tomoda C, Kihara M, Higashiyama T, Takamura Y, Miya A, Kobayashi K, Matsuzuka F, Miyauchi A (2009) S100A8 and S100A9 expression is a crucial factor for dedifferentiation in thyroid carcinoma. Anticancer Res 29(10):4157–4161
Hao J, Wang K, Yue Y, Tian T, Xu A, Xiao X, He D (2012) Selective expression of S100A11 in lung cancer and its role in regulating proliferation of adenocarcinomas cells. Mol Cell Biochem 359(1–2):323–332. doi:10.1007/s11010-011-1026-8
Howell MD, Fairchild HR, Kim BE, Bin L, Boguniewicz M, Redzic JS, Hansen KC, Leung DY (2008) Th2 cytokines act on S100/A11 to downregulate keratinocyte differentiation. J Invest Dermatol 128(9):2248–2258. doi:10.1038/jid.2008.74
Mikkelsen SE, Novitskaya V, Kriajevska M, Berezin V, Bock E, Norrild B, Lukanidin E (2001) S100A12 protein is a strong inducer of neurite outgrowth from primary hippocampal neurons. J Neurochem 79(4):767–776
Tsoporis JN, Izhar S, Proteau G, Slaughter G, Parker TG (2012) S100B-RAGE dependent VEGF secretion by cardiac myocytes induces myofibroblast proliferation. J Mol Cell Cardiol 52(2):464–473. doi:10.1016/j.yjmcc.2011.08.015
Riuzzi F, Sorci G, Donato R (2011) S100B protein regulates myoblast proliferation and differentiation by activating FGFR1 in a bFGF-dependent manner. J Cell Sci 124(14):2389–2400. doi:10.1242/jcs.084491
Riuzzi F, Sorci G, Beccafico S, Donato R (2012) S100B engages RAGE or bFGF/FGFR1 in myoblasts depending on its own concentration and myoblast density. Implications for muscle regeneration. PLoS ONE 7(1):e28700. doi:10.1371/journal.pone.0028700
Arumugam T, Simeone DM, Schmidt AM, Logsdon CD (2004) S100P stimulates cell proliferation and survival via receptor for activated glycation end products (RAGE). J Biol Chem 279(7):5059–5065. doi:10.1074/jbc.M310124200
Basu GD, Azorsa DO, Kiefer JA, Rojas AM, Tuzmen S, Barrett MT, Trent JM, Kallioniemi O, Mousses S (2008) Functional evidence implicating S100P in prostate cancer progression. Int J Cancer 123(2):330–339. doi:10.1002/ijc.23447
Acknowledgments
The authors would like to apologise for the numerous studies, which have significantly improved our understanding of the role of S100 proteins in motility/migration, but could not be included in this work owing to journal limits on the number of references.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Gross, S.R., Sin, C.G.T., Barraclough, R. et al. Joining S100 proteins and migration: for better or for worse, in sickness and in health. Cell. Mol. Life Sci. 71, 1551–1579 (2014). https://doi.org/10.1007/s00018-013-1400-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00018-013-1400-7