BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Characterization of calumenin in mouse heart

  • Sahoo, Sanjaya Kumar (Department of Life Science and Systems Biology Research Center, Gwangju Institute of Science and Technology (GIST)) ;
  • Kim, Do-Han (Department of Life Science and Systems Biology Research Center, Gwangju Institute of Science and Technology (GIST))
  • Published : 2010.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Calumenin is a multiple EF-hand $Ca^{2+}$-binding protein located in the endo/sarcoplasmic reticulum of mammalian hearts. Calumenin belongs to the CREC family of $Ca^{2+}$-binding proteins having multiple EF-hands. $Ca^{2+}$ homeostasis in the sarcoplasmic reticulum (SR) of mammalian hearts is maintained by RyR2, SERCA2 and other associated SR resident proteins. Evidence suggests that calumenin interacts with RyR2 and SERCA2, and therefore changes in the expression of calumenin could alter $Ca^{2+}$ cycling in mouse heart. In this review, current knowledge of the biochemical and functional roles of calumenin in mouse heart is described.

Keywords

References

  1. Bootman, M. D., Collins, T. J., Peppiatt, C. M., Prothero, L. S., MacKenzie, L., De Smet, P., Travers, M., Tovey, S. C., Seo, J. T. and Berridge, M. J. (2001) Calcium signaling-an overview. Semin. Cell Dev. Biol. 12, 3-10 https://doi.org/10.1006/scdb.2000.0211
  2. Carafoli, E. (1987) Intracellular calcium homeostasis. Annu. Rev. Biochem. 56, 395-433 https://doi.org/10.1146/annurev.bi.56.070187.002143
  3. Endo, M. (2006) Calcium ion as a second messenger with special reference to excitation-contraction coupling. J. Pharmacol. Sciences 100, 519-524 https://doi.org/10.1254/jphs.CPJ06004X
  4. Sato, Y., Ferguson, D. G., Sako, H., Dorn II, G. W., Kadambi, V. J., Yatani, A., Hoit, B. D., Walsh, R. A. and Kranias, E. G. (1998) Cardiac-specific overexpression of mouse cardiac calsequestrin is associated with depressed cardiovascular function and hypertrophy in transgenic Mice. J. Biol. Chem. 273, 28470-28477 https://doi.org/10.1074/jbc.273.43.28470
  5. Nakamura, K., Robertson, M., Liu, G., Dickie, P., Nakamura, K., Guo, J. Q., Duff, H. J., Opas, M., Kavanagh, K. and Michalak, M. (2001) Complete heart block and sudden death in mice overexpressing calreticulin. J. Clin. Invest. 107, 1245-1253 https://doi.org/10.1172/JCI12412
  6. Yoshida, M., Minamisawa, S., Shimura, M., Komazaki, S., Kume, H., Zhang, M., Matsumura, K., Nishi, M., Saito, M., Saeki, Y., Ishikawa, Y., Yanagisawa, T. and Takeshima, H. (2005) Impaired $Ca^{2+}$ store functions in skeletal and cardiac muscle cells from sarcalumenin-deficient mice. J. Biol. Chem. 280, 3500-3506 https://doi.org/10.1074/jbc.M406618200
  7. Gregory, K. N., Ginsburg, K. S., Bodi, I., Hahn, H., Marreez, Y. M. A., Song, Q., Padmanabhan, P. A., Mitton, B. A., Waggoner, J. R., Del Monte, F., Park, W. J., Dorn II, G. W., Bers, D. M. and Kranias, E. G. (2006) Histidinerich Ca binding protein: a regulator of sarcoplasmic reticulum calcium sequestration and cardiac function. J. Mol. Cell. Cardiol. 40, 653-665 https://doi.org/10.1016/j.yjmcc.2006.02.003
  8. Sahoo, S. and Kim, D. H. (2008) Calumenin interacts with SERCA2 in rat cardiac sarcoplasmic reticulum. Mol. Cells. 26, 265-269
  9. Sahoo, S. K., Kim, T., Kang, G. B., Lee, J. G., Eom, S. H. and Kim, D. H. (2009) Characterization of calumenin-SERCA2 interaction in mouse cardiac sarcoplasmic reticulum. J. Biol. Chem. 284, 31109-31121 https://doi.org/10.1074/jbc.M109.031989
  10. Yabe, D., Nakamura, T., Kanazawa, N., Tashiro, K. and Honjo, T. (1997) Calumenin, a $Ca^{2+}$-binding protein retained in the endoplasmic reticulum with a novel carboxyl-terminal sequence, HDEF. J. Biol. Chem. 272, 18232-18239 https://doi.org/10.1074/jbc.272.29.18232
  11. Vorum, H., Liu, X., Madsen, P., Rasmussen, H. H. and Honore, B. (1998) Molecular cloning of a cDNA encoding human calumenin, expression in Escherichia coli and analysis of its $Ca^{2+}$-binding activity. Biochim. Biophys. Acta. 1386, 121-131 https://doi.org/10.1016/S0167-4838(98)00089-2
  12. Jung, D. H., Mo, S. H. and Kim, D. H. (2006) Calumenin, a multiple EF-hands $Ca^{2+}$-binding protein, interacts with ryanodine receptor-1 in rabbit skeletal sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 343, 34-42 https://doi.org/10.1016/j.bbrc.2006.02.115
  13. Honore, B. and Vorum, H. (2000) The CREC family, a novel family of multiple EF-hand, low-affinity $Ca^{2+}$-binding proteins localised to the secretory pathway of mammalian cells. FEBS Lett. 466, 11-18 https://doi.org/10.1016/S0014-5793(99)01780-9
  14. Hseu, M. J., Yen, C. H. and Tzeng, M. C. (1999) Crocalbin: a new calcium-binding protein that is also a binding protein for crotoxin, a neurotoxic phospholipase A2. FEBS Lett. 445, 440-444 https://doi.org/10.1016/S0014-5793(99)00177-5
  15. Hseu, M. J., Yen, C. Y., Tseng, C. C. and Tzeng, M. C. (1997) Purification and partial amino acid sequence of a novel protein of the reticulocalbin family. Biochem. Biophys. Res. Commun. 239, 18-22 https://doi.org/10.1006/bbrc.1997.7416
  16. Jung, D. H. and Kim, D. H. (2004) Characterization of isoforms and genomic organization of mouse calumenin. Gene 327, 185-194 https://doi.org/10.1016/j.gene.2003.10.014
  17. Szebenyi, D. M. and Moffat, K. (1986) The refined structure of vitamin D-dependent calcium-binding protein from bovine intestine. J. Biol. Chem. 261, 8761-8777
  18. Ozawa, M. and Muramatsu, T. (1993) Reticulocalbin, a novel endoplasmic reticulum resident $Ca^{2+}$-binding protein with multiple EF-hand motifs and a carboxyl-terminal HDEL sequence. J. Biol. Chem. 268, 699-705
  19. Cooper, C. R., Graves, B., Pruitt, F., Chaib, H., Lynch, J. E., Cox, A. K., Sequeria, L., van Golen, K. L., Evans, A. and Czymmek, K. (2008) Novel surface expression of reticulocalbin 1 on bone endothelial cells and human prostate cancer cells is regulated by TNF-$\alpha$. J. Cell. Biochem. 104, 2298-2309 https://doi.org/10.1002/jcb.21785
  20. Tyedmers, J., Lerner, M., Nastainczyk, W. and Zimmermann, R. (2005) Calumenin and reticulocalbin are associated with the protein translocase of the mammalian endoplasmic reticulum. J. Biol. Sci. 5, 70-75 https://doi.org/10.3923/jbs.2005.70.75
  21. Weis, K., Griffiths, G. and Lamond, A. I. (1994) The endoplasmic reticulum calcium-binding protein of 55 kDa is a novel EF-hand protein retained in the endoplasmic reticulum by a carboxyl-terminal His-Asp-Glu-Leu motif. J. Biol. Chem. 269, 19142-19150
  22. Fohlman, J., Eaker, D., Karlsoon, E. and Thesleff, S. (1976) Taipoxin, an extremely potent presynaptic neurotoxin from the venom of the Australian snake taipan (Oxyuranus s. scutellatus). Isolation, characterization, quaternary structure and pharmacological properties. Eur. J. Biochem. 68, 457-469 https://doi.org/10.1111/j.1432-1033.1976.tb10833.x
  23. Scherer, P. E., Lederkremer, G. Z., Williams, S., Fogliano, M., Baldini, G. and Lodish, H. F. (1996) Cab45, a novel $Ca^{2+}$-binding protein localized to the Golgi lumen. J. Cell. Biol. 133, 257-268 https://doi.org/10.1083/jcb.133.2.257
  24. Lam, P. P. L., Hyvarinen, K., Kauppi, M., Cosen-Binker, L., Laitinen, S., Keranen, S., Gaisano, H. Y. and Olkkonen, V. M. (2007) A cytosolic splice variant of Cab45 interacts with Munc18b and impacts on amylase secretion by pancreatic acini. Mol. Biol. Cell. 18, 2473-2480 https://doi.org/10.1091/mbc.E06-10-0950
  25. Kimura, R., Kokubo, Y., Miyashita, K., Otsubo, R., Nagatsuka, K., Otsuki, T., Sakata, T., Nagura, J., Okayama, A. and Minematsu, K. (2006) Polymorphisms in vitamin Kdependent-carboxylation-related genes influence interindividual variability in plasma protein C and protein S activities in the general population. Int. J. Hematol. 84, 387-397 https://doi.org/10.1532/IJH97.06082
  26. Gonzalez-Conejero, R., Corral, J., Roldan, V., Ferrer, F., Sanchez-Serrano, I., Sanchez-Blanco, J. J., Marin, F. and Vicente, V. (2007) The genetic interaction between VKORC1 c1173t and calumenin a29809g modulates the anticoagulant response of acenocoumarol. J. Thromb. Haemost. 5, 1701-1706 https://doi.org/10.1111/j.1538-7836.2007.02630.x
  27. Vorum, H., Hager, H., Christensen, B. M., Nielsen, S. and Honore, B. (1999) Human calumenin localizes to the secretory pathway and is secreted to the medium. Exp. Cell Res. 248, 473-481 https://doi.org/10.1006/excr.1999.4431
  28. Papp, S., Zhang, X., Szabo, E., Michalak, M. and Opas, M. (2008) Expression of endoplasmic reticulum chaperones in cardiac development. Open Cardiovasc. Med. J. 2, 31-35 https://doi.org/10.2174/1874192400802010031
  29. MacLennan, D. H. and Wong, P. T. S. (1971) Isolation of a calcium-sequestering protein from sarcoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 68, 1231-1235 https://doi.org/10.1073/pnas.68.6.1231
  30. Fan, G. C., Gregory, K. N., Zhao, W., Park, W. J. and Kranias, E. G. (2004) Regulation of myocardial function by histidine-rich, calcium-binding protein. Am. J. Physiol. Heart Circ. Physiol. 287, H1705-1711 https://doi.org/10.1152/ajpheart.01211.2003
  31. Li, Y. and Camacho, P. (2003) $Ca^{2+}$-dependent redox modulation of SERCA2b by ERp57. J. Cell. Biol. 164, 35-46
  32. Vorum, H., Jacobsen, C. and Honore, B. (2000) Calumenin interacts with serum amyloid P component. FEBS Lett. 465, 129-134 https://doi.org/10.1016/S0014-5793(99)01734-2
  33. Wallin, R., Hutson, S. M., Cain, D., Sweatt, A. and Sane, D. C. (2001) A molecular mechanism for genetic warfarin resistance in the rat. FASEB J. 15, 2542-2544 https://doi.org/10.1096/fj.01-0337fje
  34. Furie, B. and Furie, B. C. (1988) The molecular basis of blood coagulation. Cell 53, 505-518 https://doi.org/10.1016/0092-8674(88)90567-3
  35. Furie, B. and Furie, B. C. (1990) Molecular basis of vitamin K-dependent $\gamma$-carboxylation. Blood 75, 1753-1762
  36. Suttie, J. W. (1985) Vitamin K-dependent carboxylase. Annu. Rev. Biochem. 54, 459-477 https://doi.org/10.1146/annurev.bi.54.070185.002331
  37. Wajih, N., Sane, D. C., Hutson, S. M. and Wallin, R. (2004) The inhibitory effect of calumenin on the vitamin K-dependent gamma-carboxylation system: characterization of the system in normal and warfarin-resistant rats. J. Biol. Chem. 279, 25276-25283 https://doi.org/10.1074/jbc.M401645200
  38. Wajih, N., Hutson, S. M. and Wallin, R. (2006) siRNA silencing of calumenin enhances functional factor IX production. Blood 108, 3757-3760 https://doi.org/10.1182/blood-2006-02-004671
  39. Hansen, G. A. W., Vorum, H., Jacobsen, C. and Honoré, B. (2009) Calumenin but not reticulocalbin forms a $Ca^{2+}$-dependent complex with thrombospondin-1. A potential role in haemostasis and thrombosis. Mol. Cell. Biochem 320, 25-33 https://doi.org/10.1007/s11010-008-9895-1
  40. Bornstein, P. (2001) Thrombospondins as matricellular modulators of cell function. J. Clin. Invest. 107, 929-934 https://doi.org/10.1172/JCI12749
  41. Nakazawa, T., Nakajima, A., Seki, N., Okawa, A., Kato, M., Moriya, H., Amizuka, N., Einhorn, T. A. and Yamazaki, M. (2004) Gene expression of periostin in the early stage of fracture healing detected by cDNA microarray analysis. J. Orthop. Res. 22, 520-525 https://doi.org/10.1016/j.orthres.2003.10.007
  42. Grzeskowiak, R., Witt, H., Drungowski, M., Thermann, R., Hennig, S., Perrot, A., Osterziel, K. J., Klingbiel, D., Scheid, S. and Spang, R. (2003) Expression profiling of human idiopathic dilated cardiomyopathy. Cardiovasc. Res. 59, 400-411 https://doi.org/10.1016/S0008-6363(03)00426-7
  43. Wu, W., Tang, X., Hu, W., Lotan, R., Hong, W. K. and Mao, L. (2002) Identification and validation of metastasisassociated proteins in head and neck cancer cell lines by two-dimensional electrophoresis and mass spectrometry Clin. Exp. Metastasis 19, 319-326 https://doi.org/10.1023/A:1015515119300
  44. Ding, S. J., Li, Y., Shao, X. X., Zhou, H., Zeng, R., Tang, Z. Y. and Xia, Q. C. (2004) Proteome analysis of hepatocellular carcinoma cell strains, MHCC97-H and MHCC97-L, with different metastasis potentials. Proteomics 4, 982-994 https://doi.org/10.1002/pmic.200300653
  45. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P. and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 https://doi.org/10.1016/j.cell.2006.09.026
  46. Beausoleil, S. A., Villén, J., Gerber, S. A., Rush, J. and Gygi, S. P. (2006) A probability-based approach for highthroughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24, 1285-1292 https://doi.org/10.1038/nbt1240
  47. Shah, K. and Shokat, K. M. (2002) A chemical genetic screen for direct v-Src substrates reveals ordered assembly of a retrograde signaling pathway. Chem. Biol. 9, 35-47 https://doi.org/10.1016/S1074-5521(02)00086-8

Cited by

  1. CALibrating the CALumenin gene: New insights in overcoming the vascular CALcification CALamity? vol.84, 2015, https://doi.org/10.1016/j.yjmcc.2015.04.014
  2. Calumenin has a role in the alleviation of ER stress in neonatal rat cardiomyocytes vol.439, pp.3, 2013, https://doi.org/10.1016/j.bbrc.2013.08.087
  3. Ca-Dependent Folding of Human Calumenin vol.11, pp.3, 2016, https://doi.org/10.1371/journal.pone.0151547
  4. Calumenin contributes to ER-Ca2+ homeostasis in bronchial epithelial cells expressing WT and F508del mutated CFTR and to F508del-CFTR retention vol.62, 2017, https://doi.org/10.1016/j.ceca.2017.01.011
  5. Ca2+ signalling in the Golgi apparatus vol.50, pp.2, 2011, https://doi.org/10.1016/j.ceca.2011.01.006
  6. The microRNA-132/212 family fine-tunes multiple targets in Angiotensin II signalling in cardiac fibroblasts vol.16, pp.4, 2015, https://doi.org/10.1177/1470320314539367
  7. Is There a Malignant Progression Associated with a Linear Change in Protein Expression Levels from Normal Canine Mammary Gland to Metastatic Mammary Tumors? vol.10, pp.10, 2011, https://doi.org/10.1021/pr200112q
  8. Proteomics approach to examine the cardiotoxic effects of Nemopilema nomurai Jellyfish venom vol.128, 2015, https://doi.org/10.1016/j.jprot.2015.07.008
  9. Novel identification of matrix proteins involved in calcitic biomineralization vol.116, 2015, https://doi.org/10.1016/j.jprot.2015.01.002
  10. Modulation of mouse macrophage proteome induced by Toxoplasma gondii tachyzoites in vivo vol.109, pp.6, 2011, https://doi.org/10.1007/s00436-011-2435-z
  11. Defining a Conformational Consensus Motif in Cotransin-Sensitive Signal Sequences: A Proteomic and Site-Directed Mutagenesis Study vol.10, pp.3, 2015, https://doi.org/10.1371/journal.pone.0120886
  12. Spatio-temporal expression analysis of the calcium-binding protein calumenin in the rodent brain vol.202, 2012, https://doi.org/10.1016/j.neuroscience.2011.11.069
  13. Fibulin-1C, C1 Esterase Inhibitor and Glucose Regulated Protein 75 Interact with the CREC Proteins, Calumenin and Reticulocalbin vol.10, pp.7, 2015, https://doi.org/10.1371/journal.pone.0132283
  14. Zebrafish vitamin K epoxide reductases: expression in vivo, along extracellular matrix mineralization and under phylloquinone and warfarin in vitro exposure vol.41, pp.3, 2015, https://doi.org/10.1007/s10695-015-0043-z