An Update to Calcium Binding Proteins

  • Chapter
  • First Online:
Calcium Signaling

Abstract

Ca2+ binding proteins (CBP) are of key importance for calcium to play its role as a pivotal second messenger. CBP bind Ca2+ in specific domains, contributing to the regulation of its concentration at the cytosol and intracellular stores. They also participate in numerous cellular functions by acting as Ca2+ transporters across cell membranes or as Ca2+-modulated sensors, i.e. decoding Ca2+ signals. Since CBP are integral to normal physiological processes, possible roles for them in a variety of diseases has attracted growing interest in recent years. In addition, research on CBP has been reinforced with advances in the structural characterization of new CBP family members. In this chapter we have updated a previous review on CBP, covering in more depth potential participation in physiopathological processes and candidacy for pharmacological targets in many diseases. We review intracellular CBP that contain the structural EF-hand domain: parvalbumin, calmodulin, S100 proteins, calcineurin and neuronal Ca2+ sensor proteins (NCS). We also address intracellular CBP lacking the EF-hand domain: annexins, CBP within intracellular Ca2+ stores (paying special attention to calreticulin and calsequestrin), proteins that contain a C2 domain (such as protein kinase C (PKC) or synaptotagmin) and other proteins of interest, such as regucalcin or proprotein convertase subtisilin kexins (PCSK). Finally, we summarise the latest findings on extracellular CBP, classified according to their Ca2+ binding structures: (i) EF-hand domains; (ii) EGF-like domains; (iii) ɣ-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.

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

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517–529

    Article  CAS  PubMed  Google Scholar 

  2. 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  CAS  PubMed  Google Scholar 

  3. Yáñez M, Gil-Longo J, Campos-Toimil M (2012) Calcium binding proteins. Adv Exp Med Biol 740:461–482

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  5. 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  CAS  PubMed  Google Scholar 

  6. Henzi T, Schwaller B (2015) Antagonistic regulation of parvalbumin expression and mitochondrial calcium handling capacity in renal epithelial cells. PLoS One 10:e0142005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Caillard O, Moreno H, Schwaller B, Celio MR, Marty A (2000) Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc Natl Acad Sci 97:13372–13377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Estebanez L, Hoffmann D, Voigt BC, Poulet JFA (2017) Parvalbumin-expressing GABAergic neurons in primary motor cortex signal reaching. Cell Rep 20:308–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O'Shea DJ et al (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477:171–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Inan M, Petros TJ, Anderson SA (2013) Losing your inhibition: linking cortical GABAergic interneurons to schizophrenia. Neurobiol Dis 53:36–48

    Article  CAS  PubMed  Google Scholar 

  11. Zikopoulos B, Barbas H (2013) Altered neural connectivity in excitatory and inhibitory cortical circuits in autism. Front Hum Neurosci 7:609

    Article  PubMed  PubMed Central  Google Scholar 

  12. Hu H, Gan J, Interneurons JP (2014) Fast-spiking, parvalbumin(+) GABAergic interneurons: from cellular design to microcircuit function. Science 345:1255263

    Article  PubMed  CAS  Google Scholar 

  13. Hashemi E, Ariza J, Rogers H, Noctor SC, Martínez-Cerdeño V (2017) The number of parvalbumin-expressing interneurons is decreased in the medial prefrontal cortex in autism. Cereb Cortex 27:1931–1943

    PubMed  Google Scholar 

  14. Steullet P, Cabungcal JH, Coyle J, Didriksen M, Gill K, Grace AA et al (2017) Oxidative stress-driven parvalbumin interneuron impairment as a common mechanism in models of schizophrenia. Mol Psychiatry 22:936–943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Brisch R, Bielau H, Saniotis A, Wolf R, Bogerts B, Krell D et al (2015) Calretinin and parvalbumin in schizophrenia and affective disorders: a mini-review, a perspective on the evolutionary role of calretinin in schizophrenia, and a preliminary post-mortem study of calretinin in the septal nuclei. Front Cell Neurosci 9:393

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Soghomonian JJ, Zhang K, Reprakash S, Blatt GJ (2017) Decreased parvalbumin mRNA levels in cerebellar purkinje cells in autism. Autism Res 10:1787–1796

    Article  PubMed  Google Scholar 

  17. Zou D, Chen L, Deng D, Jiang D, Dong F, McSweeney C et al (2016) DREADD in parvalbumin interneurons of the dentate gyrus modulates anxiety, social interaction and memory extinction. Curr Mol Med 16:91–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cammarota M, Losi G, Chiavegato A, Zonta M, Carmignoto G (2013) Fast spiking interneuron control of seizure propagation in a cortical slice model of focal epilepsy. J Physiol 591:807–822

    Article  CAS  PubMed  Google Scholar 

  19. Schevon CA, Weiss SA, McKhann G Jr, Goodman RR, Yuste R, Emerson RG et al (2012) Evidence of an inhibitory restraint of seizure activity in humans. Nat Commun 3:1060

    Article  PubMed  CAS  Google Scholar 

  20. Krook-Magnuson E, Armstrong C, Oijala M, Soltesz I (2013) On-demand optogenetic control of spontaneous seizures in temporal lobe epilepsy. Nat Commun 4:1376

    Article  PubMed  CAS  Google Scholar 

  21. Paz JT, Davidson TJ, Frechette ES, Delord B, Parada I, Peng K et al (2013) Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat Neurosci 16:64–70

    Article  CAS  PubMed  Google Scholar 

  22. Sessolo M, Marcon I, Bovetti S, Losi G, Cammarota M, Ratto GM et al (2015) Parvalbumin-positive inhibitory interneurons oppose propagation but favor generation of focal epileptiform activity. J Neurosci 35:9544–9557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Berg EM, Bertuzzi M, Ampatzis K (2018) Complementary expression of calcium binding proteins delineates the functional organization of the locomotor network. Brain Struct Funct 223:2181–2196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Shamgar L, Ma L, Schmitt N, Haitin Y, Peretz A, Wiener R et al (2006) Calmodulin is essential for cardiac IKS channel gating and assembly: impaired function in long-QT mutations. Circ Res 98:1055–1063

    Article  CAS  PubMed  Google Scholar 

  25. Ciampa EJ, Welch RC, Vanoye CG, George AL Jr (2011) KCNE4 juxtamembrane region is required for interaction with calmodulin and for functional suppression of KCNQ1. J Biol Chem 286:4141–4149

    Article  CAS  PubMed  Google Scholar 

  26. Chang A, Abderemane-Ali F, Hura GL, Rossen ND, Gate RE, Minor DL Jr (2018) A calmodulin c-lobe Ca2+-dependent switch governs Kv7 channel function. Neuron 97:836–852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Crotti L, Johnson CN, Graf E, De Ferrari GM, Cuneo BF, Ovadia M et al (2013) Calmodulin mutations associated with recurrent cardiac arrest in infants. Circulation 127:1009–1017

    Article  CAS  PubMed  Google Scholar 

  28. Makita N, Yagihara N, Crotti L, Johnson CN, Beckmann BM, Roh MS et al (2014) Novel calmodulin mutations associated with congenital arrhythmia susceptibility. Circ Cardiovasc Genet 7:466–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Yamamoto Y, Makiyama T, Harita T, Sasaki K, Wuriyanghai Y, Hayano M et al (2017) Allele-specific ablation rescues electrophysiological abnormalities in a human iPS cell model of long-QT syndrome with a CALM2 mutation. Hum Mol Genet 26:1670–1677

    Article  CAS  PubMed  Google Scholar 

  30. Marsman RF, Barc J, Beekman L, Alders M, Dooijes D, van den Wijngaard A et al (2014) A mutation in CALM1 encoding calmodulin in familial idiopathic ventricular fibrillation in childhood and adolescence. J Am Coll Cardiol 63:259–266

    Article  CAS  PubMed  Google Scholar 

  31. Li T, Yi L, Hai L, Ma H, Tao Z, Zhang C et al (2018) The interactome and spatial redistribution feature of Ca2+ receptor protein calmodulin reveals a novel role in invadopodia-mediated invasion. Cell Death Dis 9:292

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. McDonald KS (2018) Jack-of-many-trades: discovering new roles for troponin C. J Physiol 596(19):4553–4554. https://doi.org/10.1113/JP276790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  34. Trybus KM (1994) Role of myosin light chains. J Muscle Res Cell Motil 15:587–594

    Article  CAS  PubMed  Google Scholar 

  35. Kampourakis T, Sun YB, Irving M (2016) Myosin light chain phosphorylation enhances contraction of heart muscle via structural changes in both thick and thin filaments. Proc Natl Acad Sci U S A 113:E3039–E3047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  37. 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  CAS  PubMed  Google Scholar 

  38. 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  CAS  PubMed  Google Scholar 

  39. Gross SR, Sin CG, Barraclough R, Rudland PS (2014) Joining S100 proteins and migration: for better or for worse, in sickness and in health. Cell Mol Life Sci 71:1551–1579

    Article  CAS  PubMed  Google Scholar 

  40. Donato R, Sorci G, Giambanco I (2017) S100A6 protein: functional roles. Cell Mol Life Sci 74:2749–2760

    Article  CAS  PubMed  Google Scholar 

  41. **a C, Braunstein Z, Toomey AC, Zhong J, Rao X (2018) S100 proteins as an important regulator of macrophage inflammation. Front Immunol 8:1908

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Zimmer DB, Wright Sadosky P, Weber DJ (2003) Molecular mechanisms of S100-target protein interactions. Microsc Res Tech 60:552–559

    Article  CAS  PubMed  Google Scholar 

  43. Eckert RL, Broome AM, Ruse M, Robinson N, Ryan D, Lee K (2004) S100 proteins in the epidermis. J Invest Dermatol 123:23–33

    Article  CAS  PubMed  Google Scholar 

  44. Donato R, Sorci G, Riuzzi F, Arcuri C, Bianchi R, Brozzi F et al (2009) S100B’s double life: intracellular regulator and extracellular signal. Biochim Biophys Acta 1793:1008–1022

    Article  CAS  PubMed  Google Scholar 

  45. He H, Li J, Weng S, Li M, Yu Y (2009) S100A11: diverse function and pathology corresponding to different target proteins. Cell Biochem Biophys 55:117–126

    Article  CAS  PubMed  Google Scholar 

  46. Sherbet GV (2009) Metastasis promoter S100A4 is a potentially valuable molecular target for cancer therapy. Cancer Lett 280:15–30

    Article  CAS  PubMed  Google Scholar 

  47. 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 447:81–91

    Article  CAS  PubMed  Google Scholar 

  48. Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ et al (2013) Functions of S100 proteins. Curr Mol Med 13:24–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Brockett AT, Kane GA, Monari PK, Briones BA, Vigneron PA, Barber GA et al (2018) Evidence supporting a role for astrocytes in the regulation of cognitive flexibility and neuronal oscillations through the Ca2+ binding protein S100β. PLoS One 13:e0195726

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Sakatani S, Seto-Ohshima A, Shinohara Y, Yamamoto Y, Yamamoto H, Itohara S et al (2008) Neuralactivity-dependent release of S100β from astrocytes enhances kainate-induced gamma oscillations in vivo. J Neurosci 28:10928–10936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Diaz-Romero J, Nesic D (2017) S100A1 and S100B: calcium sensors at the cross-roads of multiple chondrogenic pathways. J Cell Physiol 232:1979–1987

    Article  CAS  PubMed  Google Scholar 

  52. Wang T, Huo X, Chong Z, Khan H, Liu R, Wang T (2018) A review of S100 protein family in lung cancer. Clin Chim Acta 476:54–59

    Article  CAS  PubMed  Google Scholar 

  53. Tian T, Li X, Hua Z, Ma J, Liu Z, Chen H et al (2017) S100A1 promotes cell proliferation and migration and is associated with lymph node metastasis in ovarian cancer. Discov Med 23:235–245

    PubMed  Google Scholar 

  54. Chen X, Liu X, Lang H, Zhang S, Luo Y, Zhang J (2015) S100 calcium-binding protein A6 promotes epithelial-mesenchymal transition through b-catenin in pancreatic cancer cell line. PLoS One 10:e0121319

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Belter B, Haase-Kohn C, Pietzsch J (2017) Biomarkers in malignant melanoma: recent trends and critical perspective. In: Ward WH, Farma JM (eds) Cutaneous melanoma: etiology and therapy. Codon Publications, Brisbane

    Google Scholar 

  56. Bresnick AR, Weber DJ, Zimmer DB (2015) S100 proteins in cancer. Nat Rev Cancer 15:96–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Tesarova P, Kalousova M, Zima T, Tesar V (2016) HMGB1, S100 proteins and other RAGE ligands in cancer-markers, mediators and putative therapeutic targets. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 160:1–10

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  59. 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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  61. Parra V, Rothermel BA (2017) Calcineurin signaling in the heart: the importance of time and place. J Mol Cell Cardiol 103:121–136

    Article  CAS  PubMed  Google Scholar 

  62. Shah SZ, Hussain T, Zhao D, Yang L (2012) A central role for calcineurin in protein misfolding neurodegenerative diseases. Cell Mol Life Sci 74:1061–1074

    Article  CAS  Google Scholar 

  63. Pongs O, Lindemeier J, Zhu XR, Theil T, Engelkamp D, Krah-Jentgens I et al (1993) Frequenin – a novel calcium-binding protein that modulates synaptic efficacy in the Drosophila nervous system. Neuron 11:15–28

    Article  CAS  PubMed  Google Scholar 

  64. Burgoyne RD, Haynes LP (2015) Sense and specificity in neuronal calcium signalling. Biochim Biophys Acta 1853:1921–1932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Angelats E, Requesens M, Aguinaga D, Kreutz MR, Franco R, Navarro G (2018) Neuronal calcium and cAMP cross-talk mediated by cannabinoid CB1 receptor and EF-hand calcium sensor interactions. Front Cell Dev Biol 6:67

    Article  PubMed  PubMed Central  Google Scholar 

  67. 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  CAS  PubMed  Google Scholar 

  68. Kaeser PS, Regehr WG (2014) Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release. Annu Rev Physiol 76:333–363

    Article  CAS  PubMed  Google Scholar 

  69. Romanov RA, Alpár A, Hökfelt T, Harkany T (2017) Molecular diversity of corticotropin-releasing hormone mRNA-containing neurons in the hypothalamus. J Endocrinol 232:R161–R172

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 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  CAS  PubMed  PubMed Central  Google Scholar 

  75. Raynal P, Pollard HB (1994) Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim Biophys Acta 1197:63–93

    Article  CAS  PubMed  Google Scholar 

  76. Gerke V, Creutz CE, Moss SE (2005) Annexins: linking Ca2þ signalling to membrane dynamics. Nat Rev Mol Cell Biol 6:449–461

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  78. D’Acunto CW, Gbelcova H, Festa M, Ruml T (2014) The complex understanding of annexin A1 phosphorylation. Cell Signal 26:173–178

    Article  PubMed  CAS  Google Scholar 

  79. Leoni G, Nusrat A (2016) Annexin A1: shifting the balance towards resolution and repair. Biol Chem 397:971–979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Christmas P, Callaway J, Fallon J, Jones J, Haigler HT (1991) Selective secretion of annexin-1, a protein without a signal sequence, by the human prostate-gland. J Biol Chem 266:2499–2507

    CAS  PubMed  Google Scholar 

  81. Guo C, Liu S, Sun M (2013b) Potential role of Anxa1 in cáncer. Future Oncol 9:1773–1793

    Article  CAS  PubMed  Google Scholar 

  82. Tu Y, Johnstone CN, Stewart AG (2017) Annexin A1 influences in breast cancer: controversies on contributions to tumour, host and immunoediting processes. Pharmacol Res 119:278–288

    Article  CAS  PubMed  Google Scholar 

  83. Boudhraa Z, Bouchon B, Viallard C, D’Incan M, Degoul F (2016) Annexin A1 localization and its relevance to cancer. Clin Sci 130:205–220

    Article  CAS  Google Scholar 

  84. Yan Tu Y, Johnstone CN, Stewart AG (2017) Annexin A1 influences in breast cancer: Controversies on contributions to tumour, host and immunoediting processes. Pharmacol Res 119:278–288

    Article  PubMed  CAS  Google Scholar 

  85. Chen L, Lv F, Pei L (2014) Annexin 1: a glucocorticoid-inducible protein that modulates inflammatory pain. Eur J Pain 18:338–347

    Article  CAS  PubMed  Google Scholar 

  86. Sugimoto MA, Vago JP, Teixeira MM, Sousa LP (2016) Annexin A1 and the resolution of inflammation: modulation of neutrophil recruitment, apoptosis, and clearance. J Immunol Res 2016:8239258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Yang YH, Morand E, Leech M (2013) Annexin A1: potential for glucocorticoid sparing in RA. Nat Rev Rheumatol 9:595–603

    Article  CAS  PubMed  Google Scholar 

  88. Qin C, Yang YH, May L, Gao X, Stewart AG, Tu Y et al (2015) Cardioprotective potential of annexin-A1 mimetics in myocardial infarction. Pharmacol Ther 148:47–65

    Article  CAS  PubMed  Google Scholar 

  89. Luo M, Hajjar KA (2013) Annexin A2 system in human biology: cell surface and beyond. Semin Thromb Hemost 39:338–346

    Article  CAS  PubMed  Google Scholar 

  90. Xu XH, Pan W, Kang LH, Feng H, Song YQ (2015) Association of annexin A2 with cancer development. Oncol Rep 33:2121–2128

    Article  CAS  PubMed  Google Scholar 

  91. Wang C, Lin C (2014a) Annexin A2: its molecular regulation and cellular expression in cancer development. Dis Markers 2014:308976

    PubMed  PubMed Central  Google Scholar 

  92. Liu X, Ma D, **g X, Wang B, Yang W, Qiu W (2015) Overexpression of ANXA2 predicts adverse outcomes of patients with malignant tumors: a systematic review and meta-analysis. Med Oncol 32:392

    Article  PubMed  CAS  Google Scholar 

  93. Tanida S, Mizoshita T, Ozeki K, Katano T, Kataoka H, Kamiya T et al (2015) Advances in refractory ulcerative colitis treatment: a new therapeutic target, Annexin A2. World J Gastroenterol 21:8776–8786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Cañas F, Simonin L, Couturaud F, Renaudineau Y (2015) Annexin A2 autoantibodies in thrombosis and autoimmune diseases. Thromb Res 135:226–230

    Article  PubMed  CAS  Google Scholar 

  95. Wu N, Liu S, Guo C, Hou Z, Sun MZ (2013) The role of annexin A3 playing in cancers. Clin Transl Oncol 15:106–110

    Article  CAS  PubMed  Google Scholar 

  96. Matsuzaki S, Serada S, Morimoto A, Ueda Y, Yoshino K, Kimura T et al (2014) Annexin A4 is a promising therapeutic target for the treatment of platinum-resistant cancers. Expert Opin Ther Targets 18:403–414

    Article  CAS  PubMed  Google Scholar 

  97. Wei B, Guo C, Liu S, Sun MZ (2015) Annexin A4 and cancer. Clin Chim Acta 447:72–78

    Article  CAS  PubMed  Google Scholar 

  98. Peng B, Guo C, Guan H, Liu S, Sun MZ (2014) Annexin A5 as a potential marker in tumors. Clin Chim Acta 427:42–48

    Article  CAS  PubMed  Google Scholar 

  99. Bouter A, Carmeille R, Gounou C, Bouvet F, Degrelle SA, Evain-Brion D et al (2015) Review: Annexin-A5 and cell membrane repair. Placenta 36:S43–S49

    Article  CAS  PubMed  Google Scholar 

  100. Carmeille R, Degrelle SA, Plawinski L, Bouvet F, Gounou C, Evain-Brion D, Brisson AR, Bouter A (2015) Annexin-A5 promotes membrane resealing in human trophoblasts. Biochim Biophys Acta 1853:2033–2044

    Article  CAS  PubMed  Google Scholar 

  101. Udry S, Aranda F, Latino O, de Larrañaga G (2013) Annexins and recurrent pregnancy loss. Medicina (B Aires) 73:495–500

    CAS  Google Scholar 

  102. Enrich C, Rentero C, Grewal T (2017) Annexin A6 in the liver: from the endocytic compartment to cellular physiology. Biochim Biophys Acta 1864:933–946

    Article  CAS  Google Scholar 

  103. Guo C, Liu S, Greenaway F, Sun MZ (2013a) Potential role of annexin A7 in cancers. Clin Chim Acta 423:83–89

    Article  CAS  PubMed  Google Scholar 

  104. Wang J, Guo C, Liu S, Qi H, Yin Y, Liang R et al (2014b) Annexin A11 in disease. Clin Chim Acta 431:164–168

    Article  CAS  PubMed  Google Scholar 

  105. Coe H, Michalak M (2009) Calcium binding chaperones of the endoplasmic reticulum. Gen Physiol Biophys 28:F96–F103

    PubMed  Google Scholar 

  106. Gutierrez T, Simmen T (2018) Endoplasmic reticulum chaperones tweak the mitochondrial calcium rheostat to control metabolism and cell death. Cell Calcium 70:64–75

    Article  CAS  PubMed  Google Scholar 

  107. Lu YC, Weng WC, Lee H (2015) Functional roles of calreticulin in cancer biology. Biomed Res Int 2015:526524

    PubMed  PubMed Central  Google Scholar 

  108. Zamanian M, Veerakumarasivam A, Abdullah S, Rosli R (2013) Calreticulin and cancer. Pathol Oncol Res 19:149–154

    Article  CAS  PubMed  Google Scholar 

  109. Nakamura K, Zuppini A, Arnaudeau S, Lynch J, Ahsan I, Krause R et al (2001) Functional specialization of calreticulin domains. J Cell Biol 154:961–972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. 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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  112. 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  CAS  PubMed  Google Scholar 

  113. 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

    CAS  PubMed  Google Scholar 

  114. Clinton A, McMullin MF (2016) The Calreticulin gene and myeloproliferative neoplasms. J Clin Pathol 69:841–845

    Article  CAS  PubMed  Google Scholar 

  115. Eggleton P, Bremer E, Dudek E, Michalak M (2016) Calreticulin, a therapeutic target? Expert Opin Ther Targets 20:1137–1147

    Article  CAS  PubMed  Google Scholar 

  116. Lievremont JP, Rizzuto R, Hendershot L, Meldolesi J (1997) BiP: a major chaperone protein of the endoplasmic reticulum lumen, plays a direct and important role in the storage of the rapidly exchanging pool of Ca2+. J Biol Chem 272:30873–30879

    Article  CAS  PubMed  Google Scholar 

  117. Taiyab A, Sreedhar AS, Rao CM (2009) Hsp90 inhibitors: GA and 17AAG, lead to ER stress-induced apoptosis in rat histiocytoma. Biochem Pharmacol 78:142–152

    Article  CAS  PubMed  Google Scholar 

  118. Narindrasorasak S, Yao P, Sarkar B (2003) Protein disulfide isomerase, a multifunctional protein chaperone, shows copper-binding activity. Biochem Biophys Res Commun 311:405–414

    Article  CAS  PubMed  Google Scholar 

  119. Xu S, Sankar S, Neamati N (2014) Protein disulfide isomerase: a promising target for cancer therapy. Drug Discov Today 19:222–240

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. 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 

  122. 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  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Gaburjakova M, Bal NC, Gaburjakova J, Periasamy M (2013) Functional interaction between calsequestrin and ryanodine receptor in the heart. Cell Mol Life Sci 70:2935–2945

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Glukhov AV, Kalyanasundaram A, Lou Q, Hage LT, Hansen BJ, Belevych AE et al (2015) Calsequestrin 2 deletion causes sinoatrial node dysfunction and atrial arrhythmias associated with altered sarcoplasmic reticulum calcium cycling and degenerative fibrosis within the mouse atrial pacemaker complex1. Eur Heart J 36:686–697

    Article  CAS  PubMed  Google Scholar 

  127. 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  CAS  PubMed  PubMed Central  Google Scholar 

  128. Guarnier FA, Michelucci A, Serano M, Pietrangelo L, Pecorai C, Boncompagni S et al (2018) Aerobic training prevents heatstrokes in calsequestrin-1 knockout mice by reducing oxidative stress. Oxidative Med Cell Longev 2018:4652480

    Article  CAS  Google Scholar 

  129. Nishizuka Y (1998) The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334:661–665

    Article  Google Scholar 

  130. Kikkawa U, Kishimoto A, Nishizuka Y (1989) The protein kinase C family: heterogeneity and its implications. Annu Rev Biochem 58:31–44

    Article  CAS  PubMed  Google Scholar 

  131. Stahelin RV (2009) Lipid binding domains: more than simple lipid effectors. J Lipid Res 50:S299–S304

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  135. 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

    Article  CAS  PubMed  Google Scholar 

  136. 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  CAS  PubMed  Google Scholar 

  137. Mochly-Rosen D, Das K, Grimes KV (2012) Protein kinase C, an elusive therapeutic target? Nat Rev Drug Discov 11:937–957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. 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  CAS  PubMed  Google Scholar 

  139. Jackman SL, Turecek J, Belinsky JE, Regehr WG (2016) The calcium sensor synaptotagmin 7 is required for synaptic facilitation. Nature 529:88–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Fernandez I, Araç D, Ubach J, Gerber SH, Shin O, Gao Y et al (2001) Three-dimensional structure of the synaptotagmin 1 C2B-domain: synaptotagmin 1 as a phospholipid binding machine. Neuron 32:1057–1069

    Article  CAS  PubMed  Google Scholar 

  141. Fernández-Chacón R, Königstorfer A, Gerber SH, García J, Matos MF, Stevens CF et al (2001) Synaptotagmin I functions as a calcium regulator of release probability. Nature 410:41–49

    Article  PubMed  Google Scholar 

  142. Johnson CP, Chapman ER (2010) Otoferlin is a calcium sensor that directly regulates SNARE-mediated membrane fusion. J Cell Biol 191:187–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Pangrsic T, Reisinger E, Moser T (2012) Otoferlin: a multi-C2 domain protein essential for hearing. Trends Neurosci 35:671–680

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  145. 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  CAS  PubMed  PubMed Central  Google Scholar 

  146. Marques R, Maia CJ, Vaz C, Correia S, Socorro S (2014) The diverse roles of calcium-binding protein regucalcin in cell biology: from tissue expression and signalling to disease. Cell Mol Life Sci 71:93–111

    Article  CAS  PubMed  Google Scholar 

  147. Yamaguchi M (2012) Role of regucalcin in brain calcium signaling: involvement in aging. Integr Biol (Camb) 4:825–837

    Article  CAS  Google Scholar 

  148. Yamaguchi M, Murata T (2013) Involvement of regucalcin in lipid metabolism and diabetes. Metab Clin Exp 62:1045–1051

    Article  CAS  PubMed  Google Scholar 

  149. Yamaguchi M (2013) Suppressive role of regucalcin in liver cell proliferation: involvement in carcinogenesis. Cell Prolif 46:243–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Yamaguchi M (2015) Involvement of regucalcin as a suppressor protein in human carcinogenesis: insight into the gene therapy. J Cancer Res Clin Oncol 141:1333–1341

    Article  CAS  PubMed  Google Scholar 

  151. Seidah NG, Chrétien M (1999) Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. Brain Res 848:45–62

    Article  CAS  PubMed  Google Scholar 

  152. Bergeron N, Phan BA, Ding Y, Fong A, Kraussn RM (2015) Proprotein convertase subtilisin/kexin type 9 inhibition: a new therapeutic mechanism for reducing cardiovascular disease risk. Circulation 132:1648–1666

    Article  CAS  PubMed  Google Scholar 

  153. Kadio B, Yaya S, Basak A, Djè K, Gomes J, Mesenge C (2016) Calcium role in human carcinogenesis: a comprehensive analysis and critical review of literature. Cancer Metastasis Rev 35:391–411

    Article  CAS  PubMed  Google Scholar 

  154. Couture F, Kwiatkowska A, Dory YL, Day R (2015) Therapeutic uses of furin and its inhibitors: a patent review. Expert Opin Ther Pat 25:379–396

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  156. Colella M, Gerbino A, Hofer AM, Curci S (2016) Recent advances in understanding the extracellular calcium-sensing receptor. F1000Res 5:2535

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  158. Chazin WJ (2011) Relating form and function of EF-hand calcium binding proteins. Acc Chem Res 44:171–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Martínez J, Cristóvão JS, Sánchez R, Gasset M, Gomes CM (2018) Preparation of amyloidogenic aggregates from EF-hand β-parvalbumin and S100 proteins. Methods Mol Biol 1779:167–179

    Article  PubMed  CAS  Google Scholar 

  160. Denessiouk K, Permyakov S, Denesyuk A, Permyakov E, Johnson MS (2014) Two structural motifs within canonical EF-hand calcium-binding domains identify five different classes of calcium buffers and sensors. PLoS One 9:e109287

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  161. Murphy-Ullrich JE, Sage EH (2014) Revisiting the matricellular concept. Matrix Biol 37:1–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Wang H, Workman G, Chen S, Barker TH, Ratner BD, Sage EH et al (2006) Secreted protein acidic and rich in cysteine (SPARC/osteonectin/BM-40) binds to fibrinogen fragments D and E, but not to native fibrinogen. Matrix Biol 25:20–26

    Article  PubMed  CAS  Google Scholar 

  163. Bradshaw AD (2012) Diverse biological functions of the SPARC family of proteins. Int J Biochem Cell Biol 44:480–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. 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  CAS  PubMed  Google Scholar 

  165. Papapanagiotou A, Sgourakis G, Karkoulias K, Raptis D, Parkin E, Brotzakis P et al (2018) Osteonectin as a screening marker for pancreatic cancer: a prospective study. J Int Med Res 46:2769–2779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. 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  CAS  PubMed  Google Scholar 

  167. Vaz J, Ansari D, Sasor A, Andersson R (2015) SPARC: a potential prognostic and therapeutic target in pancreatic cancer. Pancreas 44:1024–1035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Murphy LA, Ramirez EA, Trinh VT, Herman AM, Anderson VC, Brewster JL (2011) Endoplasmic reticulum stress or mutation of an EF-hand Ca2+-binding domain directs the FKBP65 rotamase to an ERAD-based proteolysis. Cell Stress Chaperones 16:607–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Ishikawa Y, Holden P, Bächinger HP (2017) Heat shock protein 47 and 65-kDa FK506-binding protein weakly but synergistically interact during collagen folding in the endoplasmic reticulum. J Biol Chem 292:17216–17224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Wang CK, Ghani HA, Bundock A, Weidmann J, Harvey PJ, Edwards IA et al (2018) Calcium-mediated allostery of the EGF fold. ACS Chem Biol 13:1659–1667

    Article  CAS  PubMed  Google Scholar 

  171. Engel J (1989) EGF-like domains in extracellular matrix proteins: localized signals for growth and differentiation? FEBS Lett 251:1–7

    Article  CAS  PubMed  Google Scholar 

  172. 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  CAS  PubMed  Google Scholar 

  173. 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 

  174. Rose-Martel M, Smiley S, Hincke MT (2015) Novel identification of matrix proteins involved in calcitic biomineralization. J Proteome 116:81–96

    Article  CAS  Google Scholar 

  175. Hu P, Luo BH (2018) The interface between the EGF1 and EGF2 domains is critical in integrin affinity regulation. J Cell Biochem 119(9):7264–7273. https://doi.org/10.1002/jcb.26921

    Article  CAS  PubMed  Google Scholar 

  176. Balzar M, Briaire-de Bruijn IH, Rees-Bakker HA, Prins FA, Helfrich W, de Leij L et al (2001) Epidermal growth factor-like repeats mediate lateral and reciprocal interactions of Ep-CAM molecules in homophilic adhesions. Mol Cell Biol 21:2570–2580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Saha S, Boyd J, Werner JM, Knott V, Handford PA, Campbell ID et al (2001) Solution structure of the LDL receptor EGF-AB pair: a paradigm for the assembly of tandem calcium binding EGF domains. Structure 9:451–456

    Article  CAS  PubMed  Google Scholar 

  178. Wildhagen KC, Lutgens E, Loubele ST, ten Cate H, Nicolaes GA (2011) The structure-function relationship of activated protein C. Lessons from natural and engineered mutations. Thromb Haemost 106:1034–1045

    Article  CAS  PubMed  Google Scholar 

  179. Robertson I, Jensen S, Handford P (2011) TB domain proteins: evolutionary insights into the multifaceted roles of fibrillins and LTBPs. Biochem J 433:263–276

    Article  CAS  PubMed  Google Scholar 

  180. Andersen OM, Dagil R, Kragelund BB (2013) New horizons for lipoprotein receptors: communication by β-propellers. J Lipid Res 54:2763–2774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Jensen SA, Handford PA (2016) New insights into the structure, assembly and biological roles of 10-12 nm connective tissue microfibrils from fibrillin-1 studies. Biochem J 473:827–838

    Article  CAS  PubMed  Google Scholar 

  182. 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  CAS  PubMed  PubMed Central  Google Scholar 

  183. Wang F, Li B, Lan L, Li L (2015) C596G mutation in FBN1 causes Marfan syndrome with exotropia in a Chinese family. Mol Vis 21:194–200

    PubMed  PubMed Central  Google Scholar 

  184. Garvie CW, Fraley CV, Elowe NH, Culyba EK, Lemke CT, Hubbard BK et al (2016) Point mutations at the catalytic site of PCSK9 inhibit folding, autoprocessing, and interaction with the LDL receptor. Protein Sci 25:2018–2027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  186. Cristiani A, Maset F, De Toni L, Guidolin D, Sabbadin D, Strapazzon G, Moro S, De Filippis V, Foresta C (2014) Carboxylation-dependent conformational changes of human osteocalcin. Front Biosci 19:1105–1116

    Article  CAS  Google Scholar 

  187. Palta S, Saroa R, Palta A (2014) Overview of the coagulation system. Indian J Anaesth 58:515–523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Zhao D, Wang J, Liu Y, Liu X (2015) Expressions and clinical significance of serum bone Gla-protein, bone alkaline phosphatase and C-terminal telopeptide of type I collagen in bone metabolism of patients with osteoporosis. Pak J Med Sci 31:91–94

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  190. Viegas CS, Simes DC, Laizé V, Williamson MK, Price PA, Cancela ML (2008) Gla-rich protein (GRP), a new vitamin K-dependent protein identified from sturgeon cartilage and highly conserved in vertebrates. J Biol Chem 283:36655–36664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Tie JK, Carneiro JD, ** DY, Martinhago CD, Vermeer C, Stafford DW (2016) Characterization of vitamin K-dependent carboxylase mutations that cause bleeding and nonbleeding disorders. Blood 127:1847–1855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Persson E, Madsen JJ, Olsen OH (2014) The length of the linker between the epidermal growth factor-like domains in factor VIIa is critical for a productive interaction with tissue factor. Protein Sci 23:1717–1727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  194. Sumarheni S, Hong SS, Josserand V, Coll JL, Boulanger P, Schoehn G et al (2014) Human full-length coagulation factor X and a GLA domain-derived 40-merpolypeptide bind to different regions of the adenovirus serotype 5 hexoncapsomer. Hum Gene Ther 25:339–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  196. Egorina EM, Sovershaev MA, Osterud B (2008) Regulation of tissue factor procoagulant activity by post-translational modifications. Thromb Res 122:831–837

    Article  CAS  PubMed  Google Scholar 

  197. Czogalla KJ, Watzka M, Oldenburg J (2015) Structural modeling insights into human VKORC1 phenotypes. Nutrients 7:6837–6851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Zhang YT, Tang ZY (2014) Research progress of warfarin-associated vascular calcification and its possible therapy. J Cardiovasc Pharmacol 63:76–82

    Article  PubMed  CAS  Google Scholar 

  199. Kapustin AN, Schoppet M, Schurgers LJ, Reynolds JL, McNair R, Heiss A et al (2017) Prothrombin loading of vascular smooth muscle cell-derived exosomes regulates coagulation and calcification. Arterioscler Thromb Vasc Biol 37:e22–e32

    Article  CAS  PubMed  Google Scholar 

  200. Siltari A, Vapaatalo H (2018) Vascular calcification, vitamin K and warfarin therapy – possible or plausible connection? Basic Clin Pharmacol Toxicol 122:19–24

    Article  CAS  PubMed  Google Scholar 

  201. Wallin R, Cain D, Hutson SM, Sane DC, Loeser R (2000) Modulation of the binding of matrix Gla protein (MGP) to bone morphogenetic protein-2 (BMP-2). Thromb Haemost 84:1039–1044

    Article  CAS  PubMed  Google Scholar 

  202. Lomashvili KA, Wang X, Wallin R, O’Neill WC (2011) Matrix Gla protein metabolism in vascular smooth muscle and role in uremic vascular calcification. J Biol Chem 286:28715–28722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  203. Sheng K, Zhang P, Lin W, Cheng J, Li J, Chen J (2017) Association of Matrix Gla protein gene (rs1800801, rs1800802, rs4236) polymorphism with vascular calcification and atherosclerotic disease: a meta-analysis. Sci Rep 7:8713

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  204. Luo G, Ducy P, McKee MD, Pinero GJ, Loyer E, Behringer RR et al (1997) Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386:78–81

    Article  CAS  PubMed  Google Scholar 

  205. Klezovitch O, Vasioukhin V (2015) Cadherin signaling: kee** cells in touch. F1000Res 4(F1000 Faculty Rev):550

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  207. 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  CAS  PubMed  Google Scholar 

  208. Gaengel K, Genové G, Armulik A, Betsholtz C (2009) Endothelial-mural cell signalling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 29:630–638

    Article  CAS  PubMed  Google Scholar 

  209. Blaschuk OW (2015) N-cadherin antagonists as oncology therapeutics. Philos Trans R Soc B 370:20140039

    Article  CAS  Google Scholar 

  210. Jeanes A, Gottardi CJ, Yap AS (2008) Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene 27:6920–6929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Wong SHM, Fang CM, Chuah LH, Leong CO, Ngai SC (2018) E-cadherin: Its dysregulation in carcinogenesis and clinical implications. Crit Rev Oncol Hematol 121:11–22

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  213. Varki A, Cummings RD, Esko JD, Stanley P, Hart GW, Aebi M et al (2017) Essentials of glycobiology, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  214. Aretz J, Wamhoff EC, Hanske J, Heymann D, Rademacher C (2014) Computational and experimental prediction of human C-type lectin receptor druggability. Front Immunol 5:323

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  216. Abdian PL, Caramelo JJ, Ausmees N, Zorreguieta A (2013) RapA2 is a calcium-binding lectin composed of two highly conserved cadherin-like domains that specifically recognize Rhizobium leguminosarum acidic exopolysaccharides. J Biol Chem 288:2893–2904

    Article  CAS  PubMed  Google Scholar 

  217. Bravo R, Parra V, Gatica D, Rodriguez AE, Torrealba N, Paredes F et al (2013) Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int Rev Cell Mol Biol 301:215–290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Cambi A, Figdor C (2009) Necrosis: C-type lectins sense cell death. Curr Biol 19:R375–R378

    Article  CAS  PubMed  Google Scholar 

  219. Bellande K, Bono JJ, Savelli B, Jamet E, Canut H (2017) Plant lectins and lectin receptor-like kinases: how do they sense the outside? Int J Mol Sci 18:E1164

    Article  PubMed  CAS  Google Scholar 

  220. Zou J, Jiang JY, Yang JJ (2017) Molecular basis for modulation of metabotropic glutamate receptors and their drug actions by extracellular Ca2+. Int J Mol Sci 18:672

    Article  PubMed Central  CAS  Google Scholar 

  221. Peterlik M, Kállay E, Cross HS (2013) Calcium nutrition and extracellular calcium sensing: relevance for the pathogenesis of osteoporosis, cancer and cardiovascular diseases. Nutrients 5:302–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  223. Lopez-Fernandez I, Schepelmann M, Brennan SC, Yarova PL, Riccardi D (2015) The calcium-sensing receptor: one of a kind. Exp Physiol 100:1392–1399

    Article  CAS  PubMed  Google Scholar 

  224. Conigrave AD, Ward DT (2013) Calcium-sensing receptor (CaSR): pharmacological properties and signaling pathways. Best Pract Res Clin Endocrinol Metab 27:315–331

    Article  CAS  PubMed  Google Scholar 

  225. Hannan FM, Babinsky VN, Thakker RV (2016) Disorders of the calcium-sensing receptor and partner proteins: insights into the molecular basis of calcium homeostasis. J Mol Endocrinol 57:R127–R142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  226. Riccardi D, Kemp PJ (2012) The calcium-sensing receptor beyond extracellular calcium homeostasis: conception, development, adult physiology, and disease. Rev Physiol 74:271–297

    Article  CAS  Google Scholar 

  227. Jones BL, Smith SM (2016) Calcium-sensing receptor: a key target for extracellular calcium signaling in neurons. Front Physiol 7:116

    PubMed  PubMed Central  Google Scholar 

  228. Nemeth EF, Shoback D (2013) Calcimimetic and calcilytic drugs for treating bone and mineral-related disorders. Best Pract Res Clin Endocrinol Metab 27:373–384

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  230. Jiang Y, Huang Y, Wong HC, Zhou Y, Wang X, Yang J et al (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  CAS  PubMed  PubMed Central  Google Scholar 

  231. Samardzic J (ed) (2018) GABA and glutamate. New developments in neurotransmission research. Intech Open, London

    Google Scholar 

  232. Willard SS, Koochekpour S (2013) Glutamate, glutamate receptors, and downstream signaling pathways. Int J Biol Sci 9:948–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  233. Jacobson LH, Vlachou S, Slattery DA, Li X, Cryan JF (2018) The gamma-aminobutyric acid B receptor in depression and reward. Biol Psychiatry 83:963–976

    Article  CAS  PubMed  Google Scholar 

  234. Benarroch EE (2012) GABAB receptors: structure, functions, and clinical implications. Neurology 78:578–584

    Article  CAS  PubMed  Google Scholar 

Download references

Author Contribution

JE was responsible for the writing of Sect. 8.2; he also participated in the drafting of the Introduction and Concluding Remarks sections. MY was responsible for the writing of Sect. 8.2. TMCP and JGL were responsible for the writing of Sect. 8.4. DAM contributed throughout, provided focus and flow to the various sections of the review, and oversaw/edited written English. MCT was responsible for the writing of Sect. 8.3; he also participated in the writing of the Introduction and Concluding Remarks sections and in the coordination of all authors.

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

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Elíes, J., Yáñez, M., Pereira, T.M.C., Gil-Longo, J., MacDougall, D.A., Campos-Toimil, M. (2020). An Update to Calcium Binding Proteins. In: Islam, M. (eds) Calcium Signaling. Advances in Experimental Medicine and Biology, vol 1131. Springer, Cham. https://doi.org/10.1007/978-3-030-12457-1_8

Download citation

Publish with us

Policies and ethics

Navigation