Skip to main content

Calcium Binding Proteins

  • Chapter
  • First Online:
Calcium Signaling

Abstract

The role of Ca2+ as a key and pivotal second messenger in cells depends largely on a wide number of heterogeneous so-called calcium binding proteins (CBP), which have the ability to bind this ion in specific domains. CBP contribute to the control of Ca2+ concentration in the cytosol and participate in numerous cellular functions by acting as Ca2+ transporters across cell membranes or as Ca2+-modulated sensors, i.e., decoding Ca2+ signals. In this chapter we review the main Ca2+-modulated CBP, starting with those intracellular CBP that contain the structural EF-hand domain: parvalbumin, calmodulin, S100 proteins and calcineurin. Then, we address intracellular CBP lacking the EF-hand domain: CBP within intracellular Ca2+ stores (paying special attention to calreticulin and calsequestrin), annexins and proteins that contain a C2 domain, such as protein kinase C (PKC) or sinaptotagmin. Finally, extracellular CBP have been classified in six groups, according to their Ca2+ binding structures: (i) EF-hand domains; (ii) EGF-like domains; (iii) γ-carboxyl glutamic acid (GLA)-rich domains; (iv) cadherin domains; (v) Ca2+-dependent (C)-type lectin-like domains; (vi) Ca2+-binding pockets of family C G-protein-coupled receptors. For all proteins, we briefly review their structure, location and function and additionally their potential as pharmacological targets in several human diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 299.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Carafoli E, Santella L, Branca D, Brini M (2001) Generation, control, and processing of ­cellular calcium signals. Crit Rev Biochem Mol Biol 36:107–260

    Article  PubMed  CAS  Google Scholar 

  2. Permyakov EA, Kretsinger RH (2011) Calcium binding proteins. Wiley, Hoboken

    Google Scholar 

  3. Kretsinger RH, Nockolds CE (1973) Carp muscle calcium-binding protein. II. Structure determination and general description. J Biol Chem 248:3313–3326

    PubMed  CAS  Google Scholar 

  4. Lewit-Bentley A, Rety S (2000) EF-hand calcium-binding proteins. Curr Opin Struct Biol 10:637–643

    Article  PubMed  CAS  Google Scholar 

  5. Tsigelny I, Shindyalov IN, Bourne PE, Sudhof TC, Taylor P (2000) Common EF-hand motifs in cholinesterases and neuroligins suggest a role for Ca2+ binding in cell surface associations. Protein Sci 9:180–185

    Article  PubMed  CAS  Google Scholar 

  6. Milner-White EJ (1999) The N-terminal domain of MDM2 resembles calmodulin and its relatives. J Mol Biol 292:957–963

    Article  PubMed  CAS  Google Scholar 

  7. van Asselt EJ, Dijkstra AJ, Kalk KH, Takacs B, Keck W, Dijkstra BW (1999) Crystal structure of Escherichia coli lytic transglycosylase Slt35 reveals a lysozyme-like catalytic domain with an EF-hand. Structure 7:1167–1180

    Article  PubMed  Google Scholar 

  8. Nakayama N, Kawasaki H, Kretsinger R (2000) Evolution of EF-hand proteins. In: Carafoli E, Krebs J (eds) Calcium homeostasis, topics in biological inorganic chemistry. Springer, Berlin, pp 29–58

    Google Scholar 

  9. Skelton NJ, Kordel J, Akke M, Forsen S, Chazin WJ (1994) Signal transduction versus buffering activity in Ca2+-binding proteins. Nat Struct Biol 1:239–245

    Article  PubMed  CAS  Google Scholar 

  10. Holmes KC (1996) Muscle proteins–their actions and interactions. Curr Opin Struct Biol 6:781–789

    Article  PubMed  CAS  Google Scholar 

  11. Arif SH (2009) A Ca2+-binding protein with numerous roles and uses: parvalbumin in molecular biology and physiology. Bioessays 31:410–421

    Article  PubMed  CAS  Google Scholar 

  12. Deuticke HJ (1934) Über die Sedimentationskonstante von Muskelproteinen. Hoppe Seylers Z Physiol Chem 224:216–228

    Article  CAS  Google Scholar 

  13. Pechere JF (1968) Muscular parvalbumins as homologous proteins. Comp Biochem Physiol 24:289–295

    Article  PubMed  CAS  Google Scholar 

  14. Schaub MC, Heizmann CW (2008) Calcium, troponin, calmodulin, S100 proteins: from myocardial basics to new therapeutic strategies. Biochem Biophys Res Commun 369:247–264

    Article  PubMed  CAS  Google Scholar 

  15. Heizmann CW (1984) Parvalbumin, an intracellular calcium-binding protein; distribution, properties and possible roles in mammalian cells. Experientia 40:910–921

    Article  PubMed  CAS  Google Scholar 

  16. Gerday C, Gillis JM (1976) Proceedings: the possible role of parvalbumins in the control of contraction. J Physiol 258:96P–97P

    PubMed  CAS  Google Scholar 

  17. Baude A, Bleasdale C, Dalezios Y, Somogyi P, Klausberger T (2007) Immunoreactivity for the GABAA receptor alpha1 subunit, somatostatin and connexin36 distinguishes axoaxonic, basket, and bistratified interneurons of the rat hippocampus. Cereb Cortex 17:2094–2107

    Article  PubMed  Google Scholar 

  18. Cheung WY (1970) Cyclic 3′,5′-nucleotide phosphodiesterase. Demonstration of an activator. Biochem Biophys Res Commun 38:533–538

    Article  PubMed  CAS  Google Scholar 

  19. Kakiuchi S, Yamazaki R (1970) Calcium dependent phosphodiesterase activity and its activating factor (PAF) from brain studies on cyclic 3′,5′-nucleotide phosphodiesterase (3). Biochem Biophys Res Commun 41:1104–1110

    Article  PubMed  CAS  Google Scholar 

  20. Cohen P, Klee CB (1988) Calmodulin. Elsevier, Amsterdam

    Google Scholar 

  21. Jurado LA, Chockalingam PS, Jarrett HW (1999) Apocalmodulin. Physiol Rev 79:661–682

    PubMed  CAS  Google Scholar 

  22. Igarashi M, Watanabe M (2007) Roles of calmodulin and calmodulin-binding proteins in synaptic vesicle recycling during regulated exocytosis at submicromolar Ca2+ concentrations. Neurosci Res 58:226–233

    Article  PubMed  CAS  Google Scholar 

  23. Kawasaki H, Kretsinger RH (1994) Calcium-binding proteins. 1: EF-hands. Protein Profile 1:343–517

    PubMed  CAS  Google Scholar 

  24. Toutenhoofd SL, Strehler EE (2000) The calmodulin multigene family as a unique case of genetic redundancy: multiple levels of regulation to provide spatial and temporal control of calmodulin pools? Cell Calcium 28:83–96

    Article  PubMed  CAS  Google Scholar 

  25. Iwatsubo T, Nakano I, Fukunaga K, Miyamoto E (1991) Ca2+/calmodulin-dependent protein kinase II immunoreactivity in Lewy bodies. Acta Neuropathol 82:159–163

    Article  PubMed  CAS  Google Scholar 

  26. McLachlan DR, Wong L, Bergeron C, Baimbridge KG (1987) Calmodulin and calbindin D28K in Alzheimer disease. Alzheimer Dis Assoc Disord 1:171–179

    Article  PubMed  CAS  Google Scholar 

  27. Ali M, Ponchel F, Wilson KE, Francis MJ, Wu X, Verhoef A, Boylston AW, Veale DJ, Emery P, Markham AF, Lamb JR, Isaacs JD (2001) Rheumatoid arthritis synovial T cells regulate transcription of several genes associated with antigen-induced anergy. J Clin Invest 107:519–528

    Article  PubMed  CAS  Google Scholar 

  28. Perry SV, Corsi A (1958) Extraction of proteins other than myosin from the isolated rabbit myofibril. Biochem J 68:5–12

    PubMed  CAS  Google Scholar 

  29. Gillis TE, Marshall CR, Tibbits GF (2007) Functional and evolutionary relationships of troponin C. Physiol Genomics 32:16–27

    Article  PubMed  CAS  Google Scholar 

  30. Moore BW, McGregor D (1965) Chromatographic and electrophoretic fraction of soluble proteins of brain and liver. J Biol Chem 240:1647–1653

    PubMed  CAS  Google Scholar 

  31. 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 322:1111–1122

    Article  PubMed  CAS  Google Scholar 

  32. Zhou Y, Yang W, Kirberger M, Lee HW, Ayalasomayajula G, Yang JJ (2006) Prediction of EF-hand calcium-binding proteins and analysis of bacterial EF-hand proteins. Proteins 65:643–655

    Article  PubMed  CAS  Google Scholar 

  33. 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 277:4578–4590

    Article  PubMed  CAS  Google Scholar 

  34. Nishikawa T, Lee IS, Shiraishi N, Ishikawa T, Ohta Y, Nishikimi M (1997) Identification of S100b protein as copper-binding protein and its suppression of copper-induced cell damage. J Biol Chem 272:23037–23041

    Article  PubMed  CAS  Google Scholar 

  35. Donato R (2003) Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60:540–551

    Article  PubMed  CAS  Google Scholar 

  36. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS (2006) Calcium-dependent and -independent interactions of the S100 protein family. Biochem J 396:201–214

    Article  PubMed  CAS  Google Scholar 

  37. Heizmann CW, Ackermann GE, Galichet A (2007) Pathologies involving the S100 proteins and RAGE. Subcell Biochem 45:93–138

    Article  PubMed  CAS  Google Scholar 

  38. Klee CB, Krinks MH (1978) Purification of cyclic 3′,5′-nucleotide phosphodiesterase inhibitory protein by affinity chromatography on activator protein coupled to Sepharose. Biochemistry 17:120–126

    Article  PubMed  CAS  Google Scholar 

  39. Rusnak F, Mertz P (2000) Calcineurin: form and function. Physiol Rev 80:1483–1521

    PubMed  CAS  Google Scholar 

  40. Li J, Jia Z, Zhou W, Wei Q (2009) Calcineurin regulatory subunit B is a unique calcium sensor that regulates calcineurin in both calcium-dependent and calcium-independent manner. Proteins 77:612–623

    Article  PubMed  CAS  Google Scholar 

  41. Li H, Rao A, Hogan PG (2011) Interaction of calcineurin with substrates and targeting proteins. Trends Cell Biol 21:91–103

    Article  PubMed  CAS  Google Scholar 

  42. Pongs O, Lindemeier J, Zhu XR, Theil T, Engelkamp D, Krah-Jentgens I, Lambrecht HG, Koch KW, Schwemer J, Rivosecchi R, Mallart A, Galceran J, Canal I, Barbas JA, Ferrús A (1993) Frequenin -a novel calcium-binding protein that modulates synaptic efficacy in the Drosophila nervous system. Neuron 11:15–28

    Article  PubMed  CAS  Google Scholar 

  43. Burgoyne RD (2007) Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci 8:182–193

    Article  PubMed  CAS  Google Scholar 

  44. McCue HV, Haynes LP, Burgoyne RD (2010) The diversity of calcium sensor proteins in the regulation of neuronal function. Cold Spring Harb Perspect Biol 2:a004085

    Article  PubMed  CAS  Google Scholar 

  45. Braunewell KH (2005) The darker side of Ca2+ signaling by neuronal Ca2+-sensor proteins: from Alzheimer’s disease to cancer. Trends Pharmacol Sci 26:345–351

    Article  PubMed  CAS  Google Scholar 

  46. Renner M, Danielson MA, Falke JJ (1993) Kinetic control of Ca(II) signaling: tuning the ion dissociation rates of EF-hand Ca(II) binding sites. Proc Natl Acad Sci USA 90:6493–6497

    Article  PubMed  CAS  Google Scholar 

  47. Gifford JL, Walsh MP, Vogel HJ (2007) Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem J 405:199–221

    Article  PubMed  CAS  Google Scholar 

  48. Coe H, Michalak M (2009) Calcium binding chaperones of the endoplasmic reticulum. Gen Physiol Biophys 28 Spec No Focus:F96–F103

    PubMed  Google Scholar 

  49. Ashby MC, Tepikin AV (2001) ER calcium and the functions of intracellular organelles. Semin Cell Dev Biol 12:11–17

    Article  PubMed  CAS  Google Scholar 

  50. Baksh S, Michalak M (1991) Expression of calreticulin in Escherichia coli and identification of its Ca2+ binding domains. J Biol Chem 266:21458–21465

    PubMed  CAS  Google Scholar 

  51. Gelebart P, Opas M, Michalak M (2005) Calreticulin, a Ca2+-binding chaperone of the endoplasmic reticulum. Int J Biochem Cell Biol 37:260–266

    Article  PubMed  CAS  Google Scholar 

  52. Nakamura K, Zuppini A, Arnaudeau S, Lynch J, Ahsan I, Krause R, Papp S, De Smedt H, Parys JB, Muller-Esterl W, Lew DP, Krause KH, Demaurex N, Opas M, Michalak M (2001) Functional specialization of calreticulin domains. J Cell Biol 154:961–972

    Article  PubMed  CAS  Google Scholar 

  53. Villamil Giraldo AM, Lopez Medus M, Gonzalez Lebrero M, Pagano RS, Labriola CA, Landolfo L, Delfino JM, Parodi AJ, Caramelo JJ (2010) The structure of calreticulin C-terminal domain is modulated by physiological variations of calcium concentration. J Biol Chem 285:4544–4553

    Article  PubMed  CAS  Google Scholar 

  54. Arnaudeau S, Frieden M, Nakamura K, Castelbou C, Michalak M, Demaurex N (2002) Calreticulin differentially modulates calcium uptake and release in the endoplasmic reticulum and mitochondria. J Biol Chem 277:46696–46705

    Article  PubMed  CAS  Google Scholar 

  55. Trombetta ES (2003) The contribution of N-glycans and their processing in the endoplasmic reticulum to glycoprotein biosynthesis. Glycobiology 13:77R–91R

    Article  PubMed  CAS  Google Scholar 

  56. Zhu N, Wang Z (1999) Calreticulin expression is associated with androgen regulation of the sensitivity to calcium ionophore-induced apoptosis in LNCaP prostate cancer cells. Cancer Res 59:1896–1902

    PubMed  CAS  Google Scholar 

  57. MacLennan DH, Wong PT (1971) Isolation of a calcium-sequestering protein from sarcoplasmic reticulum. Proc Natl Acad Sci USA 68:1231–1235

    Article  PubMed  CAS  Google Scholar 

  58. Novák P, Soukup T (2011) Calsequestrin distribution, structure and function, its role in normal and pathological situations and the effect of thyroid hormones. A review. Physiol Res 60:439–452

    PubMed  Google Scholar 

  59. Milstein ML, Houle TD, Cala SE (2009) Calsequestrin isoforms localize to different ER subcompartments: evidence for polymer and heteropolymer-dependent localization. Exp Cell Res 315:523–534

    Article  PubMed  CAS  Google Scholar 

  60. Gyorke I, Hester N, Jones LR, Gyorke S (2004) The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys J 86:2121–2128

    Article  PubMed  Google Scholar 

  61. Qin J, Valle G, Nani A, Nori A, Rizzi N, Priori SG, Volpe P, Fill M (2008) Luminal Ca2+ regulation of single cardiac ryanodine receptors: insights provided by calsequestrin and its mutants. J Gen Physiol 131:325–334

    Article  PubMed  CAS  Google Scholar 

  62. Mitchell RD, Simmerman HK, Jones LR (1988) Ca2+ binding effects on protein conformation and protein interactions of canine cardiac calsequestrin. J Biol Chem 263:1376–1381

    PubMed  CAS  Google Scholar 

  63. Wei L, Hanna AD, Beard NA, Dulhunty AF (2009) Unique isoform-specific properties of calsequestrin in the heart and skeletal muscle. Cell Calcium 45:474–484

    Article  PubMed  CAS  Google Scholar 

  64. Gyorke S, Gyorke I, Terentyev D, Viatchenko-Karpinski S, Williams SC (2004) Modulation of sarcoplasmic reticulum calcium release by calsequestrin in cardiac myocytes. Biol Res 37:603–607

    Article  PubMed  Google Scholar 

  65. Royer L, Rios E (2009) Deconstructing calsequestrin. Complex buffering in the calcium store of skeletal muscle. J Physiol 587:3101–3111

    Article  PubMed  CAS  Google Scholar 

  66. Paolini C, Quarta M, Nori A, Boncompagni S, Canato M, Volpe P, Allen PD, Reggiani C, Protasi F (2007) Reorganized stores and impaired calcium handling in skeletal muscle of mice lacking calsequestrin-1. J Physiol 583:767–784

    Article  PubMed  CAS  Google Scholar 

  67. Pertille A, de Carvalho CL, Matsumura CY, Neto HS, Marques MJ (2010) Calcium-binding proteins in skeletal muscles of the mdx mice: potential role in the pathogenesis of Duchenne muscular dystrophy. Int J Exp Pathol 91:63–71

    Article  PubMed  CAS  Google Scholar 

  68. Lestienne P, Bataille N, Lucas-Heron B (1995) Role of the mitochondrial DNA and calmitine in myopathies. Biochim Biophys Acta 1271:159–163

    PubMed  Google Scholar 

  69. Rescher U, Gerke V (2004) Annexins -unique membrane binding proteins with diverse functions. J Cell Sci 117:2631–2639

    Article  PubMed  CAS  Google Scholar 

  70. Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371

    PubMed  CAS  Google Scholar 

  71. Moss SE, Morgan RO (2004) The annexins. Genome Biol 5:219

    Article  PubMed  Google Scholar 

  72. Geisow MJ, Fritsche U, Hexham JM, Dash B, Johnson T (1986) A consensus amino-acid sequence repeat in Torpedo and mammalian Ca2+-dependent membrane-binding proteins. Nature 320:636–638

    Article  PubMed  CAS  Google Scholar 

  73. Mishra S, Chander V, Banerjee P, Oh JG, Lifirsu E, Park WJ, Kim dH, Bandyopadhyay A (2011) Interaction of annexin A6 with alpha actinin in cardiomyocytes. BMC Cell Biol 12:7

    Article  PubMed  CAS  Google Scholar 

  74. Solito E, Nuti S, Parente L (1994) Dexamethasone-induced translocation of lipocortin (annexin) 1 to the cell membrane of U-937 cells. Br J Pharmacol 112:347–348

    PubMed  CAS  Google Scholar 

  75. Brownstein C, Falcone DJ, Jacovina A, Hajjar KA (2001) A mediator of cell surface-specific plasmin generation. Ann N Y Acad Sci 947:143–155

    Article  PubMed  CAS  Google Scholar 

  76. Fatimathas L, Moss SE (2010) Annexins as disease modifiers. Histol Histopathol 25:527–532

    PubMed  CAS  Google Scholar 

  77. Nishizuka Y (1988) The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334:661–665

    Article  PubMed  CAS  Google Scholar 

  78. Rizo J, Sudhof TC (1998) C2-domains, structure and function of a universal Ca2+-binding domain. J Biol Chem 273:15879–15882

    Article  PubMed  CAS  Google Scholar 

  79. Nalefski EA, Falke JJ (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5:2375–2390

    Article  PubMed  CAS  Google Scholar 

  80. Newton AC (2010) Protein kinase C: poised to signal. Am J Physiol Endocrinol Metab 298:E395–E402

    Article  PubMed  CAS  Google Scholar 

  81. Steinberg SF (2008) Structural basis of protein kinase C isoform function. Physiol Rev 88:1341–1378

    Article  PubMed  CAS  Google Scholar 

  82. Newton AC, Johnson JE (1998) Protein kinase C: a paradigm for regulation of protein function by two membrane-targeting modules. Biochim Biophys Acta 1376:155–172

    PubMed  CAS  Google Scholar 

  83. Giorgione JR, Lin JH, McCammon JA, Newton AC (2006) Increased membrane affinity of the C1 domain of protein kinase Cdelta compensates for the lack of involvement of its C2 domain in membrane recruitment. J Biol Chem 281:1660–1669

    Article  PubMed  CAS  Google Scholar 

  84. Breitkreutz D, Braiman-Wiksman L, Daum N, Denning MF, Tennenbaum T (2007) Protein kinase C family: on the crossroads of cell signaling in skin and tumor epithelium. J Cancer Res Clin Oncol 133:793–808

    Article  PubMed  CAS  Google Scholar 

  85. Perin MS, Fried VA, Mignery GA, Jahn R, Sudhof TC (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345:260–263

    Article  PubMed  CAS  Google Scholar 

  86. Fernandez I, Arac D, Ubach J, Gerber SH, Shin O, Gao Y, Anderson RG, Sudhof TC, Rizo J (2001) Three-dimensional structure of the synaptotagmin 1 C2B-domain: synaptotagmin 1 as a phospholipid binding machine. Neuron 32:1057–1069

    Article  PubMed  CAS  Google Scholar 

  87. Craxton M (2004) Synaptotagmin gene content of the sequenced genomes. BMC Genomics 5:43

    Article  PubMed  CAS  Google Scholar 

  88. Fernández-Chacón R, Konigstorfer A, Gerber SH, García J, Matos MF, Stevens CF, Brose N, Rizo J, Rosenmund C, Sudhof TC (2001) Synaptotagmin I functions as a calcium regulator of release probability. Nature 410:41–49

    Article  PubMed  Google Scholar 

  89. Bunney TD, Katan M (2011) PLC regulation: emerging pictures for molecular mechanisms. Trends Biochem Sci 36:88–96

    Article  PubMed  CAS  Google Scholar 

  90. Lee JC, Simonyi A, Sun AY, Sun GY (2011) Phospholipases A2 and neural membrane dynamics: implications for Alzheimer’s disease. J Neurochem 116:813–819

    Article  PubMed  CAS  Google Scholar 

  91. Brown EM, MacLeod RJ (2001) Extracellular calcium sensing and extracellular calcium ­signaling. Physiol Rev 81:239–297

    PubMed  CAS  Google Scholar 

  92. Hofer AM (2005) Another dimension to calcium signaling: a look at extracellular calcium. J Cell Sci 118:855–862

    Article  PubMed  CAS  Google Scholar 

  93. Bornstein P (2009) Matricellular proteins: an overview. J Cell Commun Signal 3:163–165

    Article  PubMed  Google Scholar 

  94. Brekken RA, Sage EH (2001) SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol 19:816–827

    Article  PubMed  CAS  Google Scholar 

  95. Busch E, Hohenester E, Timpl R, Paulsson M, Maurer P (2000) Calcium affinity, cooperativity, and domain interactions of extracellular EF-hands present in BM-40. J Biol Chem 275:25508–25515

    Article  PubMed  CAS  Google Scholar 

  96. Podhajcer OL, Benedetti L, Girotti MR, Prada F, Salvatierra E, Llera AS (2008) The role of the matricellular protein SPARC in the dynamic interaction between the tumor and the host. Cancer Metastasis Rev 27:523–537

    Article  PubMed  CAS  Google Scholar 

  97. Maurer P, Hohenester E, Engel J (1996) Extracellular calcium-binding proteins. Curr Opin Cell Biol 8:609–617

    Article  PubMed  CAS  Google Scholar 

  98. Krebs J, Heizmann CW (2007) Calcium-binding proteins and the EF-hand principle. In: Krebs J, Michalak M (eds) Calcium: a matter of life or death. Elsevier, Amsterdam, pp 51–93

    Chapter  Google Scholar 

  99. Stenflo J, Stenberg Y, Muranyi A (2000) Calcium-binding EGF-like modules in coagulation proteinases: function of the calcium ion in module interactions. Biochim Biophys Acta 1477:51–63

    Article  PubMed  CAS  Google Scholar 

  100. Handford PA (2000) Fibrillin-1, a calcium binding protein of extracellular matrix. Biochim Biophys Acta 1498:84–90

    Article  PubMed  CAS  Google Scholar 

  101. Pena F, Jansens A, van Zadelhoff G, Braakman I (2010) Calcium as a crucial cofactor for low density lipoprotein receptor folding in the endoplasmic reticulum. J Biol Chem 285:8656–8664

    Article  PubMed  CAS  Google Scholar 

  102. Cranenburg EC, Schurgers LJ, Vermeer C (2007) Vitamin K: the coagulation vitamin that became omnipotent. Thromb Haemost 98:120–125

    PubMed  CAS  Google Scholar 

  103. Ohkubo YZ, Tajkhorshid E (2008) Distinct structural and adhesive roles of Ca2+ in membrane binding of blood coagulation factors. Structure 16:72–81

    Article  PubMed  CAS  Google Scholar 

  104. Hansson K, Stenflo J (2005) Post-translational modifications in proteins involved in blood coagulation. J Thromb Haemost 3:2633–2648

    Article  PubMed  CAS  Google Scholar 

  105. Halbleib JM, Nelson WJ (2006) Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20:3199–3214

    Article  PubMed  CAS  Google Scholar 

  106. Boggon TJ, Murray J, Chappuis-Flament S, Wong E, Gumbiner BM, Shapiro L (2002) C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 296:1308–1313

    Article  PubMed  CAS  Google Scholar 

  107. Oroz J, Valbuena A, Vera AM, Mendieta J, Gomez-Puertas P, Carrion-Vazquez M (2011) Nanomechanics of the cadherin ectodomain: “canalization” by Ca2+ binding results in a new mechanical element. J Biol Chem 286:9405–9418

    Article  PubMed  CAS  Google Scholar 

  108. Cambi A, Koopman M, Figdor CG (2005) How C-type lectins detect pathogens. Cell Microbiol 7:481–488

    Article  PubMed  CAS  Google Scholar 

  109. Zelensky AN, Gready JE (2005) The C-type lectin-like domain superfamily. FEBS J 272:6179–6217

    Article  PubMed  CAS  Google Scholar 

  110. Silve C, Petrel C, Leroy C, Bruel H, Mallet E, Rognan D, Ruat M (2005) Delineating a Ca2+ binding pocket within the venus flytrap module of the human calcium-sensing receptor. J Biol Chem 280:37917–37923

    Article  PubMed  CAS  Google Scholar 

  111. Steddon SJ, Cunningham J (2005) Calcimimetics and calcilytics -fooling the calcium receptor. Lancet 365:2237–2239

    Article  PubMed  CAS  Google Scholar 

  112. Jiang Y, Huang Y, Wong HC, Zhou Y, Wang X, Yang J, Hall RA, Brown EM, Yang JJ (2010) Elucidation of a novel extracellular calcium-binding site on metabotropic glutamate receptor 1{alpha} (mGluR1{alpha}) that controls receptor activation. J Biol Chem 285:33463–33474

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manuel Campos-Toimil .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Yáñez, M., Gil-Longo, J., Campos-Toimil, M. (2012). Calcium Binding Proteins. In: Islam, M. (eds) Calcium Signaling. Advances in Experimental Medicine and Biology, vol 740. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2888-2_19

Download citation

Publish with us

Policies and ethics