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Solution structure of human Mts1 (S100A4) as determined by NMR spectroscopy.

Vallely KM, Rustandi RR, Ellis KC, Varlamova O, Bresnick AR, Weber DJ
Biochemistry 41 12670-80 (2002)
Cited: 50 times
EuropePMC logo PMID: 12379109

Abstract

Mts1 is a member of the S100 family of Ca2+-binding proteins and is implicated in promoting tumor progression and metastasis. To better understand the structure-function relationships of this protein and to begin characterizing its Ca2+-dependent interaction with protein binding targets, the three-dimensional structure of mts1 was determined in the apo state by NMR spectroscopy. As with other S100 protein family members, mts1 is a symmetric homodimer held together by noncovalent interactions between two helices from each subunit (helices 1, 4, 1', and 4') to form an X-type four-helix bundle. Each subunit of mts1 has two EF-hand Ca2+-binding domains: a pseudo-EF-hand (or S100-hand) and a typical EF-hand that are brought into proximity by a small two-stranded antiparallel beta-sheet. The S100-hand is formed by helices 1 and 2, and is similar in conformation to other members of the S100 family. In the typical EF-hand, the position of helix 3 is similar to that of another member of the S100 protein family, calcyclin (S100A6), and less like that of other S100 family members for which three-dimensional structures are available in the calcium-free state (e.g., S100B and S100A1). The differences in the position of helix 3 in the apo state of these four S100 proteins are likely due to variations in the amino acid sequence in the C-terminus of helix 4 and in loop 2 (the hinge region) and could potentially be used to subclassify the S100 protein family.

Reviews - 1m31 mentioned but not cited (1)

  1. S100 proteins as therapeutic targets. Bresnick AR. Biophys Rev 10 1617-1629 (2018)

Articles - 1m31 mentioned but not cited (10)

  1. Structure of Ca2+-bound S100A4 and its interaction with peptides derived from nonmuscle myosin-IIA. Malashkevich VN, Varney KM, Garrett SC, Wilder PT, Knight D, Charpentier TH, Ramagopal UA, Almo SC, Weber DJ, Bresnick AR. Biochemistry 47 5111-5126 (2008)
  2. Calprotectin S100A9 calcium-binding loops I and II are essential for keratinocyte resistance to bacterial invasion. Champaiboon C, Sappington KJ, Guenther BD, Ross KF, Herzberg MC. J Biol Chem 284 7078-7090 (2009)
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  6. Peptide mimetic of the S100A4 protein modulates peripheral nerve regeneration and attenuates the progression of neuropathy in myelin protein P0 null mice. Moldovan M, Pinchenko V, Dmytriyeva O, Pankratova S, Fugleholm K, Klingelhofer J, Bock E, Berezin V, Krarup C, Kiryushko D. Mol Med 19 43-53 (2013)
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Reviews citing this publication (6)

  1. Calcium-dependent and -independent interactions of the S100 protein family. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS. Biochem J 396 201-214 (2006)
  2. Binding of S100 proteins to RAGE: an update. Leclerc E, Fritz G, Vetter SW, Heizmann CW. Biochim Biophys Acta 1793 993-1007 (2009)
  3. The heavy chain has its day: regulation of myosin-II assembly. Dulyaninova NG, Bresnick AR. Bioarchitecture 3 77-85 (2013)
  4. Metastasis promoter S100A4 is a potentially valuable molecular target for cancer therapy. Sherbet GV. Cancer Lett 280 15-30 (2009)
  5. RAGE Inhibitors for Targeted Therapy of Cancer: A Comprehensive Review. Faruqui T, Khan MS, Akhter Y, Khan S, Rafi Z, Saeed M, Han I, Choi EH, Yadav DK. Int J Mol Sci 24 266 (2022)
  6. S100A6 as a Constituent and Potential Marker of Adult and Cancer Stem Cells. Leśniak W, Filipek A. Stem Cell Rev Rep 18 2699-2708 (2022)

Articles citing this publication (33)

  1. 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. Yammani RR, Carlson CS, Bresnick AR, Loeser RF. Arthritis Rheum 54 2901-2911 (2006)
  2. Dcn1 functions as a scaffold-type E3 ligase for cullin neddylation. Kurz T, Chou YC, Willems AR, Meyer-Schaller N, Hecht ML, Tyers M, Peter M, Sicheri F. Mol Cell 29 23-35 (2008)
  3. Myosin-IIA heavy-chain phosphorylation regulates the motility of MDA-MB-231 carcinoma cells. Dulyaninova NG, House RP, Betapudi V, Bresnick AR. Mol Biol Cell 18 3144-3155 (2007)
  4. Molecular mechanisms of Ca(2+) signaling in neurons induced by the S100A4 protein. Kiryushko D, Novitskaya V, Soroka V, Klingelhofer J, Lukanidin E, Berezin V, Bock E. Mol Cell Biol 26 3625-3638 (2006)
  5. S100A4 regulates macrophage chemotaxis. Li ZH, Dulyaninova NG, House RP, Almo SC, Bresnick AR. Mol Biol Cell 21 2598-2610 (2010)
  6. Evolution of the S100 family of calcium sensor proteins. Zimmer DB, Eubanks JO, Ramakrishnan D, Criscitiello MF. Cell Calcium 53 170-179 (2013)
  7. The three-dimensional solution structure of Ca(2+)-bound S100A1 as determined by NMR spectroscopy. Wright NT, Varney KM, Ellis KC, Markowitz J, Gitti RK, Zimmer DB, Weber DJ. J Mol Biol 353 410-426 (2005)
  8. S100A1: Structure, Function, and Therapeutic Potential. Wright NT, Cannon BR, Zimmer DB, Weber DJ. Curr Chem Biol 3 138-145 (2009)
  9. S100P dissociates myosin IIA filaments and focal adhesion sites to reduce cell adhesion and enhance cell migration. Du M, Wang G, Ismail TM, Gross S, Fernig DG, Barraclough R, Rudland PS. J Biol Chem 287 15330-15344 (2012)
  10. Asymmetric mode of Ca²⁺-S100A4 interaction with nonmuscle myosin IIA generates nanomolar affinity required for filament remodeling. 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. Structure 20 654-666 (2012)
  11. Coupling S100A4 to Rhotekin alters Rho signaling output in breast cancer cells. Chen M, Bresnick AR, O'Connor KL. Oncogene 32 3754-3764 (2013)
  12. Unmasking the annexin I interaction from the structure of Apo-S100A11. Dempsey AC, Walsh MP, Shaw GS. Structure 11 887-897 (2003)
  13. An oxazetidine amino acid for chemical protein synthesis by rapid, serine-forming ligations. Pusterla I, Bode JW. Nat Chem 7 668-672 (2015)
  14. Mutually antagonistic actions of S100A4 and S100A1 on normal and metastatic phenotypes. Wang G, Zhang S, Fernig DG, Martin-Fernandez M, Rudland PS, Barraclough R. Oncogene 24 1445-1454 (2005)
  15. Molecular basis of the complex formation between the two calcium-binding proteins S100A8 (MRP8) and S100A9 (MRP14). Leukert N, Sorg C, Roth J. Biol Chem 386 429-434 (2005)
  16. The Calcium-Dependent Interaction of S100B with Its Protein Targets. Zimmer DB, Weber DJ. Cardiovasc Psychiatry Neurol 2010 728052 (2010)
  17. Solution structure of the novel dispersin protein of enteroaggregative Escherichia coli. Velarde JJ, Varney KM, Inman KG, Farfan M, Dudley E, Fletcher J, Weber DJ, Nataro JP. Mol Microbiol 66 1123-1135 (2007)
  18. Downregulation of S100A4 expression by RNA interference suppresses cell growth and invasion in human colorectal cancer cells. Huang L, Xu Y, Cai G, Guan Z, Cai S. Oncol Rep 27 917-922 (2012)
  19. The C-terminal region of S100A4 is important for its metastasis-inducing properties. Zhang S, Wang G, Liu D, Bao Z, Fernig DG, Rudland PS, Barraclough R, Barraclough R. Oncogene 24 4401-4411 (2005)
  20. Crystal structure of metastasis-associated protein S100A4 in the active calcium-bound form. Pathuri P, Vogeley L, Luecke H. J Mol Biol 383 62-77 (2008)
  21. Crystal structure of the Ca(2+)-form and Ca(2+)-binding kinetics of metastasis-associated protein, S100A4. Gingras AR, Basran J, Prescott A, Kriajevska M, Bagshaw CR, Barsukov IL. FEBS Lett 582 1651-1656 (2008)
  22. A new role for PGRP-S (Tag7) in immune defense: lymphocyte migration is induced by a chemoattractant complex of Tag7 with Mts1. Dukhanina EA, Lukyanova TI, Romanova EA, Guerriero V, Gnuchev NV, Georgiev GP, Yashin DV, Sashchenko LP. Cell Cycle 14 3635-3643 (2015)
  23. Crystal structure of Ca2+ -free S100A2 at 1.6-A resolution. Koch M, Diez J, Fritz G. J Mol Biol 378 933-942 (2008)
  24. Heterodimeric interaction and interfaces of S100A1 and S100P. Wang G, Zhang S, Fernig DG, Spiller D, Martin-Fernandez M, Zhang H, Ding Y, Rao Z, Rudland PS, Barraclough R. Biochem J 382 375-383 (2004)
  25. Structure of the S100A4/myosin-IIA complex. Ramagopal UA, Dulyaninova NG, Varney KM, Wilder PT, Nallamsetty S, Brenowitz M, Weber DJ, Almo SC, Bresnick AR. BMC Struct Biol 13 31 (2013)
  26. Two functional S100A4 monomers are necessary for regulating nonmuscle myosin-IIA and HCT116 cell invasion. House RP, Pozzuto M, Patel P, Dulyaninova NG, Li ZH, Zencheck WD, Vitolo MI, Weber DJ, Bresnick AR. Biochemistry 50 6920-6932 (2011)
  27. Intrinsically disordered and aggregation prone regions underlie β-aggregation in S100 proteins. Carvalho SB, Botelho HM, Leal SS, Cardoso I, Fritz G, Gomes CM. PLoS One 8 e76629 (2013)
  28. Refined crystal structures of human Ca(2+)/Zn(2+)-binding S100A3 protein characterized by two disulfide bridges. Unno M, Kawasaki T, Takahara H, Heizmann CW, Kizawa K. J Mol Biol 408 477-490 (2011)
  29. Multilevel Changes in Protein Dynamics upon Complex Formation of the Calcium-Loaded S100A4 with a Nonmuscle Myosin IIA Tail Fragment. Pálfy G, Kiss B, Nyitray L, Bodor A. Chembiochem 17 1829-1838 (2016)
  30. The structure of Ca2+-loaded S100A2 at 1.3-Å resolution. Koch M, Fritz G. FEBS J 279 1799-1810 (2012)
  31. Solution structure and backbone dynamics of Calsensin, an invertebrate neuronal calcium-binding protein. Venkitaramani DV, Fulton DB, Andreotti AH, Johansen KM, Johansen J. Protein Sci 14 1894-1901 (2005)
  32. KAHA Ligation at Serine. Li YM, Huang YC, Liu L. Chembiochem 17 28-30 (2016)
  33. TD-11 workshop report: characterization of monoclonal antibodies to S100 proteins. Paus E, Haugen MH, Olsen KH, Flatmark K, Maelandsmo GM, Nilsson O, Röijer E, Lundin M, Fermér C, Samsonova M, Lebedin Y, Stigbrand T. Tumour Biol 32 1-12 (2011)


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