1932

Abstract

From the catalytic reactions that sustain the global oxygen, nitrogen, and carbon cycles to the stabilization of DNA processing proteins, transition metal ions and metallocofactors play key roles in biology. Although the exquisite interplay between metal ions and protein scaffolds has been studied extensively, the fact that the biological roles of the metals often stem from their placement in the interfaces between proteins and protein subunits is not always recognized. Interfacial metal ions stabilize permanent or transient protein–protein interactions, enable protein complexes involved in cellular signaling to adopt distinct conformations in response to environmental stimuli, and catalyze challenging chemical reactions that are uniquely performed by multisubunit protein complexes. This review provides a structural survey of transition metal ions and metallocofactors found in protein–protein interfaces, along with a series of selected examples that illustrate their diverse biological utility and significance.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-051013-023038
2014-05-06
2024-05-25
Loading full text...

Full text loading...

/deliver/fulltext/biophys/43/1/annurev-biophys-051013-023038.html?itemId=/content/journals/10.1146/annurev-biophys-051013-023038&mimeType=html&fmt=ahah

Literature Cited

  1. Alber BE, Colangelo CM, Dong J, Stålhandske CMV, Baird TT. 1.  et al. 1999. Kinetic and spectroscopic characterization of the gamma-carbonic anhydrase from the methanoarchaeon Methanosarcina thermophila. Biochemistry 38:13119–28 [Google Scholar]
  2. Anbar AD. 2.  2008. Elements and evolution. Science 322:1481–83 [Google Scholar]
  3. Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM. 3.  2008. Metal ions in biological catalysis: from enzyme databases to general principles. J. Biol. Inorg. Chem. 13:1205–18Reports the roles and distribution of metal ions in enzymes using the Metal-MACiE database. [Google Scholar]
  4. Andreini C, Cavallaro G, Lorenzini S, Rosato A. 4.  2013. MetalPDB: a database of metal sites in biological macromolecular structures. Nucleic Acids Res. 41:D312–19 [Google Scholar]
  5. Aravind L, Iyer LM, Koonin EV. 5.  2006. Comparative genomics and structural biology of the molecular innovations of eukaryotes. Curr. Opin. Struct. Biol. 16:409–19 [Google Scholar]
  6. Armstrong RN. 6.  2000. Mechanistic diversity in a metalloenzyme superfamily. Biochemistry 39:13625–32Discusses the functional diversity of the vicinal oxygen chelate (VOC) superfamily and its evolutionary origins. [Google Scholar]
  7. Baron MK, Boeckers TM, Vaida B, Faham S, Gingery M. 7.  et al. 2006. An architectural framework that may lie at the core of the postsynaptic density. Science 311:531–35 [Google Scholar]
  8. Baudier J, Glasser N, Gerard D. 8.  1986. Ions binding to S100 proteins. I. Calcium- and zinc-binding properties of bovine brain S100αα, S100a (αβ), and S100b (ββ) protein: Zn2+ regulates Ca2+ binding on S100b protein. J. Biol. Chem 261:8192–203 [Google Scholar]
  9. Bennett MJ, Schlunegger MP, Eisenberg D. 9.  1995. 3D domain swapping: a mechanism for oligomer assembly. Protein Sci. 4:2455–68 [Google Scholar]
  10. Bergdoll M, Eltis LD, Cameron AD, Dumas P, Bolin JT. 10.  1998. All in the family: structural and evolutionary relationships among three modular proteins with diverse functions and variable assembly. Protein Sci. 7:1661–70 [Google Scholar]
  11. Berridge MJ, Lipp P, Bootman MD. 11.  2000. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1:11–21 [Google Scholar]
  12. Bertini I, Gray HB, Stiefel EI, Valentine JS. 12.  2007. Biological Inorganic Chemistry: Structure and Reactivity Sausalito, CA: University Science Books [Google Scholar]
  13. Bertini I, Decaria L, Rosato A. 13.  2010. The annotation of full zinc proteomes. J. Biol. Inorg. Chem. 15:1071–78 [Google Scholar]
  14. Bixby KA, Nanao MH, Shen NV, Kreusch A, Bellamy H. 14.  et al. 1999. Zn2+-binding and molecular determinants of tetramerization in voltage-gated K+ channels. Nature 6:38–43 [Google Scholar]
  15. Boal AK, Rosenzweig AC. 15.  2009. Structural biology of copper trafficking. Chem. Rev. 109:4760–79 [Google Scholar]
  16. Brodin JD, Medina-Morales A, Ni T, Salgado EN, Ambroggio XI, Tezcan FA. 16.  2010. Evolution of metal selectivity in templated protein interfaces. J. Am. Chem. Soc. 132:8610–17 [Google Scholar]
  17. Brodin JD, Ambroggio XI, Tang C, Parent KN, Baker TS, Tezcan FA. 17.  2012. Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays. Nat. Chem. 4:375–82Reports a novel strategy for forming protein-based biomaterials directed by metal ions. [Google Scholar]
  18. Brown NL, Stoyanov JV, Kidd SP, Hobman JL. 18.  2003. The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 27:145–63 [Google Scholar]
  19. Buckel W, Hetzel M, Kim J. 19.  2004. ATP-driven electron transfer in enzymatic radical reactions. Curr. Opin. Chem. Biol. 8:462–67 [Google Scholar]
  20. Burgess BK, Lowe DJ. 20.  1996. Mechanism of molybdenum nitrogenase. Chem. Rev. 96:2983–3012 [Google Scholar]
  21. Cameron AD, Ridderström M, Olin B, Kavarana MJ, Creighton DJ, Mannervik B. 21.  1999. Reaction mechanism of glyoxalase I explored by an X-ray crystallographic analysis of the human enzyme in complex with a transition state analogue. Biochemistry 38:13480–90 [Google Scholar]
  22. Changela A, Chen K, Xue Y, Holschen J, Outten CE. 22.  et al. 2003. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301:1383–87 [Google Scholar]
  23. Chao Y, Fu D. 23.  2004. Thermodynamic studies of the mechanism of metal binding to the Escherichia coli zinc transporter YiiP. J. Biol. Chem. 279:17173–80 [Google Scholar]
  24. Charpentier TH, Wilder PT, Liriano MA, Varney KM, Pozharski E. 24.  et al. 2008. Divalent metal ion complexes of S100B in the absence and presence of pentamidine. J. Mol. Biol. 382:56–73 [Google Scholar]
  25. Christianson DW, Fierke CA. 25.  1996. Carbonic anhydrase: evolution of the zinc binding site by nature and by design. Acc. Chem. Res. 29:331–39 [Google Scholar]
  26. Ciszak E, Smith GD. 26.  1994. Crystallographic evidence for dual coordination around zinc in the T3R3 human insulin hexamer. Biochemistry 33:1512–17 [Google Scholar]
  27. Contreras M, Thiberge J-M, Mandrand-Berthelot M-A, Labigne A. 27.  2003. Characterization of the roles of NikR, a nickel-responsive pleiotropic autoregulator of Helicobacter pylori. Mol. Microbiol. 49:947–63 [Google Scholar]
  28. Coudray N, Valvo S, Hu M, Lasala R, Kim C. 28.  et al. 2013. Inward-facing conformation of the zinc transporter YiiP revealed by cryoelectron microscopy. Proc. Natl. Acad. Sci. USA 110:2140–45 [Google Scholar]
  29. Dabrowski MJ, Yanchunas J, Villafranca BC, Dietze EC, Schurke P, Atkins WM. 29.  1994. Supramolecular self-assembly of glutamine synthetase: mutagenesis of a novel intermolecular metal binding site required for dodecamer stacking. Biochemistry 33:14957–64 [Google Scholar]
  30. Der BS, Edwards DR, Kuhlman B. 30.  2012. Catalysis by a de novo zinc-mediated protein interface: implications for natural enzyme evolution and rational enzyme engineering. Biochemistry 51:3933–40Reports the design of a de novo designed dimer with hydrolytically active, interfacial Zn ions. [Google Scholar]
  31. Dian C, Schauer K, Kapp U, McSweeney SM, Labigne A, Terradot L. 31.  2006. Structural basis of the nickel response in Helicobacter pylori: crystal structures of HpNikR in apo and nickel-bound states. J. Mol. Biol. 361:715–30 [Google Scholar]
  32. Dobbek H, Svetlitchnyi V, Gremer L, Huber R, Meyer O. 32.  2001. Crystal structure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster. Science 293:1281–85 [Google Scholar]
  33. D'Ordine RL, Rydel TJ, Storek MJ, Sturman EJ, Moshiri F. 33.  et al. 2009. Dicamba monooxygenase: structural insights into a dynamic Rieske oxygenase that catalyzes an exocyclic monooxygenation. J. Mol. Biol. 392:481–97 [Google Scholar]
  34. Drennan CL, Heo J, Sintchak MD, Schreiter E, Ludden PW. 34.  2001. Life on carbon monoxide: X-ray structure of Rhodospirillum rubrum Ni-Fe-S carbon monoxide dehydrogenase. Proc. Natl. Acad. Sci. USA 98:11973–78 [Google Scholar]
  35. Dunn MF. 35.  2005. Zinc–ligand interactions modulate assembly and stability of the insulin hexamer—a review. Biometals 18:295–303 [Google Scholar]
  36. Dupont CL, Butcher A, Valas RE, Bourne PE, Caetano-Anollés G. 36.  2010. History of biological metal utilization inferred through phylogenomic analysis of protein structures. Proc. Natl. Acad. Sci. USA 107:10567–72Discusses the interplay between environmental metal ion bioavailability and protein evolution. [Google Scholar]
  37. Fraústo da Silva JJR, Williams RJP. 37.  2001. The Biological Chemistry of the Elements Oxford, UK: Oxford Univ. PressA comprehensive textbook that describes and discusses the roles of inorganic elements in biology.
  38. Fritz G, Botelho HM, Morozova-Roche LA, Gomes CM. 38.  2010. Natural and amyloid self-assembly of S100 proteins: structural basis of functional diversity. FEBS J. 277:4578–90 [Google Scholar]
  39. Gaskin F, Kress Y. 39.  1977. Zinc ion–induced assembly of tubulin. J. Biol. Chem. 252:6918–24 [Google Scholar]
  40. Gibrat J-F, Madej T, Bryant S. 40.  1996. Surprising similarities in structure comparison. Curr. Opin. Struct. Biol. 6:377–85 [Google Scholar]
  41. Gibson DT, Parales RE. 41.  2000. Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr. Opin. Biotechnol. 11:236–43 [Google Scholar]
  42. Hennig SE, Jeoung J-H, Goetzl S, Dobbek H. 42.  2012. Redox-dependent complex formation by an ATP-dependent activator of the corrinoid/iron-sulfur protein. Proc. Natl. Acad. Sci. USA 109:5235–40 [Google Scholar]
  43. Hopfner KP, Craig L, Moncalian G, Zinkel RA, Usui T. 43.  et al. 2002. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418:562–66 [Google Scholar]
  44. Howard JB, Rees DC. 44.  1996. Structural basis of biological nitrogen fixation. Chem. Rev. 96:2965–82 [Google Scholar]
  45. Hsin K, Sheng Y, Harding MM, Taylor P, Walkinshaw MD. 45.  2008. MESPEUS: a database of the geometry of metal sites in proteins. J. Appl. Cryst. 41:963–68 [Google Scholar]
  46. Iverson TM, Alber BE, Kisker C, Ferry JG, Rees DC. 46.  2000. A closer look at the active site of gamma-class carbonic anhydrases: high-resolution crystallographic studies of the carbonic anhydrase from Methanosarcina thermophila. Biochemistry 39:9222–31 [Google Scholar]
  47. Jahng AW, Strang C, Kaiser D, Pollard T, Pfaffinger P, Choe S. 47.  2002. Zinc mediates assembly of the T1 domain of the voltage-gated K channel 4.2. J. Biol. Chem. 277:47885–90 [Google Scholar]
  48. Jones S, Thornton JM. 48.  1996. Principles of protein–protein interactions. Proc. Natl. Acad. Sci. USA 93:13–20 [Google Scholar]
  49. Kennedy MB. 49.  2000. Signal-processing machines at the postsynaptic density. Science 290:750–54 [Google Scholar]
  50. Kim PW, Sun Z-YJ, Blacklow SC, Wagner G, Eck MJ. 50.  2003. A zinc clasp structure tethers Lck to T cell coreceptors CD4 and CD8. Science 301:1725–28 [Google Scholar]
  51. Knight MJ, Joubert MK, Plotkowski ML, Kropat J, Gingery M. 51.  et al. 2010. Zinc binding drives sheet formation by the SAM domain of diacylglycerol kinase δ. Biochemistry 49:9667–76 [Google Scholar]
  52. Komori H, Inagaki S, Yoshioka S, Aono S, Higuchi Y. 52.  2007. Crystal structure of CO-sensing transcription activator CooA bound to exogenous ligand imidazole. J. Mol. Biol. 367:864–71 [Google Scholar]
  53. Krantz BA, Sosnick TR. 53.  2001. Engineered metal binding sites map the heterogeneous folding landscape of a coiled coil. Nat. Struct. Biol. 8:1042–47 [Google Scholar]
  54. Krissinel E, Henrick K. 54.  2007. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372:774–97 [Google Scholar]
  55. Laganowsky A, Zhao M, Soriaga AB, Sawaya MR, Cascio D, Yeates TO. 55.  2011. An approach to crystallizing proteins by metal-mediated synthetic symmetrization. Protein Sci. 20:1876–90 [Google Scholar]
  56. Laity JH, Lee BM, Wright PE. 56.  2001. Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 11:39–46 [Google Scholar]
  57. Lepore BW, Ruzicka FJ, Frey PA, Ringe D. 57.  2005. The x-ray crystal structure of lysine-2,3-aminomutase from Clostridium subterminale. Proc. Natl. Acad. Sci. USA 102:13819–24 [Google Scholar]
  58. Löwe J, Li H, Downing KH, Nogales E. 58.  2001. Refined structure of αβ-tubulin at 3.5 Å resolution. J. Mol. Biol. 313:1045–57 [Google Scholar]
  59. Lu M, Chai J, Fu D. 59.  2009. Structural basis for autoregulation of the zinc transporter YiiP. Nat. Struct. Mol. Biol. 16:1063–67 [Google Scholar]
  60. Mateja A, Szlachcic A, Downing ME, Dobosz M, Mariappan M. 60.  et al. 2009. The structural basis of tail-anchored membrane protein recognition by Get3. Nature 461:361–66 [Google Scholar]
  61. Matoba Y, Bando N, Oda K, Noda M, Higashikawa F. 61.  et al. 2011. A molecular mechanism for copper transportation to tyrosinase that is assisted by a metallochaperone, caddie protein. J. Biol. Chem. 286:30219–31 [Google Scholar]
  62. Matoba Y, Kumagai T, Yamamoto A, Yoshitsu H, Sugiyama M. 62.  2006. Crystallographic evidence that the dinuclear copper center of tyrosinase is flexible during catalysis. J. Biol. Chem. 281:8981–90 [Google Scholar]
  63. Medina-Morales A, Perez A, Brodin JD, Tezcan FA. 63.  2013. In vitro and cellular self-assembly of a Zn-binding protein cryptand via templated disulfide bonds. J. Am. Chem. Soc. 135:12013–22Reports the engineering of oligomeric proteins directed by metal coordination and disulfide bonds. [Google Scholar]
  64. Ni TW, Tezcan FA. 64.  2010. Structural characterization of a microperoxidase inside a metal-directed protein cage. Angew. Chem. Int. Ed. 49:7014–18 [Google Scholar]
  65. Nogales E, Wolf SG, Downing KH. 65.  1998. Structure of the αβ tubulin dimer by electron crystallography. Nature 391:199–203 [Google Scholar]
  66. Ohana E, Hoch E, Keasar C, Kambe T, Yifrach O. 66.  et al. 2009. Identification of the Zn2+ binding site and mode of operation of a mammalian Zn2+ transporter. J. Biol. Chem. 284:17677–86 [Google Scholar]
  67. Ostendorp T, Diez J, Heizmann CW, Fritz G. 67.  2011. The crystal structures of human S100B in the zinc- and calcium-loaded state at three pH values reveal zinc ligand swapping. Biochim. Biophys. Acta 1813:1083–91 [Google Scholar]
  68. Palacios EH, Weiss A. 68.  2004. Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation. Oncogene 23:7990–8000 [Google Scholar]
  69. Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC. 69.  1998. X-ray crystal structure of the Fe-only hydroge-nase (CpI) from Clostridium pasteurianum to 1.8 Angstrom resolution. Science 282:1853–58 [Google Scholar]
  70. Pomposiello PJ, Demple B. 70.  2001. Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol. 19:109–14 [Google Scholar]
  71. Que EL, Domaille DW, Chang CJ. 71.  2008. Metals in neurobiology: probing their chemistry and biology with molecular imaging. Chem. Rev. 108:1517–49 [Google Scholar]
  72. Reddi AR, Guzman TR, Breece RM, Tiemey DL, Gibney BR. 72.  2007. Deducing the energetic cost of protein folding in zinc finger proteins using designed metallopeptides. J. Am. Chem. Soc. 129:12815–27 [Google Scholar]
  73. Rees DC, Howard JB. 73.  2000. Nitrogenase: standing at the crossroads. Curr. Opin. Chem. Biol. 4:559–66 [Google Scholar]
  74. Riechmann L, Winter G. 74.  2006. Early protein evolution: building domains from ligand-binding polypeptide segments. J. Mol. Biol. 363:460–68 [Google Scholar]
  75. Romir J, Lilie H, Egerer-Sieber C, Bauer F, Sticht H, Muller YA. 75.  2007. Crystal structure analysis and solution studies of human Lck-SH3; zinc-induced homodimerization competes with the binding of proline-rich motifs. J. Mol. Biol. 365:1417–28 [Google Scholar]
  76. Rosovitz MJ, Schuck P, Varughese M, Chopra AP, Mehra V. 76.  et al. 2003. Alanine-scanning mutations in domain 4 of anthrax toxin protective antigen reveal residues important for binding to the cellular receptor and to a neutralizing monoclonal antibody. J. Biol. Chem. 278:30936–44 [Google Scholar]
  77. Roussignol G, Ango F, Romorini S, Tu JC, Sala C. 77.  et al. 2005. Shank expression is sufficient to induce functional dendritic spine synapses in aspiny neurons. J. Neurosci. 25:3560–70 [Google Scholar]
  78. Salgado EN, Ambroggio XI, Brodin JD, Lewis RA, Kuhlman B, Tezcan FA. 78.  2010. Metal-templated design of protein interfaces. Proc. Natl. Acad. Sci. USA 107:1827–32 [Google Scholar]
  79. Salgado EN, Lewis RA, Mossin S, Rheingold AL, Tezcan FA. 79.  2009. Control of protein oligomerization symmetry by metal coordination: C2 and C3 symmetrical assemblies through CuII and NiII coordination. Inorg. Chem. 48:2726–28 [Google Scholar]
  80. Santelli E, Bankston LA, Leppla SH, Liddington RC. 80.  2004. Crystal structure of a complex between anthrax toxin and its host cell receptor. Nature 430:905–8 [Google Scholar]
  81. Schindelin H, Kisker C, Schlessman JL, Howard JB, Rees DC. 81.  1997. Structure of ADP·AIF4-stabilized nitrogenase complex and its implications for signal transduction. Nature 387:370–76 [Google Scholar]
  82. Schreiter ER, Wang SC, Zamble DB, Drennan CL. 82.  2006. NikR–operator complex structure and the mechanism of repressor activation by metal ions. Proc. Natl. Acad. Sci. USA 103:13676–81 [Google Scholar]
  83. Shelver D, Kerby RL, He Y, Roberts GP. 83.  1997. CooA, a CO-sensing transcription factor from Rhodospirillum rubrum, is a CO-binding heme protein. Proc. Natl. Acad. Sci. USA 94:11216–20 [Google Scholar]
  84. Smith GD, Swenson DC, Dodson EJ, Dodson GG, Reynolds CD. 84.  1984. Structural stability in the 4-zinc human insulin hexamer. Proc. Natl. Acad. Sci. USA 81:7093–97 [Google Scholar]
  85. Spatzal T, Aksoyoglu M, Zhang LM, Andrade SLA, Schleicher E. 85.  et al. 2011. Evidence for interstitial carbon in nitrogenase FeMo cofactor. Science 334:940 [Google Scholar]
  86. Stefer S, Reitz S, Wang F, Wild K, Pang Y-Y. 86.  et al. 2011. Structural basis for tail-anchored membrane protein biogenesis by the Get3-receptor complex. Science 333:758–62 [Google Scholar]
  87. Strozyk D, Bush AI. 87.  2006. The role of metal ions in neurology. An introduction. Neurodegenerative Diseases and Metal Ions A Sigel, H Sigel, RKO Sigel 11–7 Chichester, UK: Wiley [Google Scholar]
  88. Supuran CT. 88.  2008. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat. Rev. Drug Discov. 7:168–81 [Google Scholar]
  89. Tezcan FA, Kaiser JT, Mustafi D, Walton MY, Howard JB, Rees DC. 89.  2005. Nitrogenase complexes: multiple docking sites for a nucleotide switch protein. Science 309:1377–80 [Google Scholar]
  90. Thornalley PJ. 90.  1990. The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem. J. 269:1–11 [Google Scholar]
  91. Volbeda A, Hol WGJ. 91.  1989. Pseudo 2-fold symmetry in the copper-binding domain of arthropodan haemocyanins: possible implications for the evolution of oxygen transport proteins. J. Mol. Biol. 206:531–46 [Google Scholar]
  92. Waldron KJ, Rutherford JC, Ford D, Robinson NJ. 92.  2009. Metalloproteins and metal sensing. Nature 460:823–30A comprehensive overview of how transition metal ions are sensed inside cells. [Google Scholar]
  93. Watanabe S, Kita A, Kobayashi K, Miki K. 93.  2008. Crystal structure of the [2Fe-2S] oxidative-stress sensor SoxR bound to DNA. Proc. Natl. Acad. Sci. USA 105:4121–26 [Google Scholar]
  94. Wei Y, Fu D. 94.  2006. Binding and transport of metal ions at the dimer interface of the Escherichia coli metal transporter YiiP. J. Biol. Chem. 281:23492–502 [Google Scholar]
  95. Weinreb PH, Li S, Gao SX, Liu T, Pepinsky RB. 95.  et al. 2012. Dynamic structural changes are observed upon collagen and metal ion binding to the integrin α1 I domain. J. Biol. Chem. 287:32897–912 [Google Scholar]
  96. Wernimont AK, Huffman DL, Lamb AL, O'Halloran TV, Rosenzweig AC. 96.  2000. Structural basis for copper transfer by the metallochaperone for the Menkes/Wilson disease proteins. Nat. Struct. Biol. 7:766–71 [Google Scholar]
  97. West AL, Evans SE, González JM, Carter LG, Tsuruta H. 97.  et al. 2012. Ni(II) coordination to mixed sites modulates DNA binding of HpNikR via a long-range effect. Proc. Natl. Acad. Sci. USA 109:5633–38 [Google Scholar]
  98. Williams RJP, Fraústo Da Silva JJR. 98.  2003. Evolution was chemically constrained. J. Theor. Biol. 220:323–43 [Google Scholar]
  99. Youn H, Kerby RL, Conrad M, Roberts GP. 99.  2004. Functionally critical elements of CooA-related CO sensors. J. Bacteriol. 186:1320–29 [Google Scholar]
  100. Zhang L, Kaiser JT, Meloni G, Yang K-Y, Spatzal T. 100.  et al. 2013. The sixteenth iron in the nitrogenase MoFe protein. Agnew. Chem. Int. Ed 52:10529–32 [Google Scholar]
  101. Zimmer DB, Cornwall EH, Landar A, Song W. 101.  1995. The S100 protein family: history, function, and expression. Brain Res. Bull. 37:417–29 [Google Scholar]
/content/journals/10.1146/annurev-biophys-051013-023038
Loading
/content/journals/10.1146/annurev-biophys-051013-023038
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error