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Cellular and Molecular Life Sciences

, Volume 71, Issue 1, pp 93–111 | Cite as

The diverse roles of calcium-binding protein regucalcin in cell biology: from tissue expression and signalling to disease

  • Ricardo Marques
  • Cláudio J. Maia
  • Cátia Vaz
  • Sara Correia
  • Sílvia SocorroEmail author
Review

Abstract

Regucalcin (RGN) is a calcium (Ca2+)-binding protein widely expressed in vertebrate and invertebrate species, which is also known as senescence marker protein 30, due to its molecular weight (33 kDa) and a characteristically diminished expression with the aging process. RGN regulates intracellular Ca2+ homeostasis and the activity of several proteins involved in intracellular signalling pathways, namely, kinases, phosphatases, phosphodiesterase, nitric oxide synthase and proteases, which highlights its importance in cell biology. In addition, RGN has cytoprotective effects reducing intracellular levels of oxidative stress, also playing a role in the control of cell survival and apoptosis. Multiple factors have been identified regulating the cell levels of RGN transcripts and protein, and an altered expression pattern of this interesting protein has been found in cases of reproductive disorders, neurodegenerative diseases and cancer. Moreover, RGN is a serum-secreted protein, and its levels have been correlated with the stage of disease, which strongly suggests the usefulness of this protein as a potential biomarker for monitoring disease onset and progression. The present review aims to discuss the available information concerning RGN expression and function in distinct cell types and tissues, integrating cellular and molecular mechanisms in the context of normal and pathological conditions. Insight into the cellular actions of RGN will be a key step towards deepening the knowledge of the biology of several human diseases.

Keywords

Regucalcin SMP30 Calcium Apoptosis Oxidative stress Cell proliferation 

Notes

Acknowledgments

This work was partially supported by Portuguese Foundation for Science and Technology (FCT) under Program COMPETE (PEst-C/SAU/UI0709/2011). Ricardo Marques, Cátia Vaz and Sara Correia were funded by FCT fellowships (SFRH/BD/66875/2009, SFRH/BD/70316/2010 and SFRH/BD/60945/2009, respectively).

References

  1. 1.
    Yamaguchi M, Yamamoto T (1978) Purification of calcium binding substance from soluble fraction of normal rat liver. Chem Pharm Bull (Tokyo) 26(6):1915–1918CrossRefGoogle Scholar
  2. 2.
    Shimokawa N, Yamaguchi M (1993) Molecular cloning and sequencing of the cDNA coding for a calcium-binding protein regucalcin from rat liver. FEBS Lett 327(3):251–255PubMedCrossRefGoogle Scholar
  3. 3.
    Kondo Y, Ishigami A, Kubo S, Handa S, Gomi K, Hirokawa K, Kajiyama N, Chiba T, Shimokado K, Maruyama N (2004) Senescence marker protein-30 is a unique enzyme that hydrolyzes diisopropyl phosphorofluoridate in the liver. FEBS Lett 570(1–3):57–62PubMedCrossRefGoogle Scholar
  4. 4.
    Chakraborti S, Bahnson BJ (2010) Crystal structure of human senescence marker protein 30: insights linking structural, enzymatic, and physiological functions. Biochemistry 49(16):3436–3444PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Yamaguchi M (2000) Role of regucalcin in calcium signaling. Life Sci 66(19):1769–1780PubMedCrossRefGoogle Scholar
  6. 6.
    Kondo Y, Inai Y, Sato Y, Handa S, Kubo S, Shimokado K, Goto S, Nishikimi M, Maruyama N, Ishigami A (2006) Senescence marker protein 30 functions as gluconolactonase in l-ascorbic acid biosynthesis, and its knockout mice are prone to scurvy. Proc Natl Acad Sci USA 103(15):5723–5728PubMedCrossRefGoogle Scholar
  7. 7.
    Fujita T, Mandel JL, Shirasawa T, Hino O, Shirai T, Maruyama N (1995) Isolation of cDNA clone encoding human homologue of senescence marker protein-30 (SMP30) and its location on the X chromosome. Biochim Biophys Acta 1263(3):249–252PubMedCrossRefGoogle Scholar
  8. 8.
    Shimokawa N, Matsuda Y, Yamaguchi M (1995) Genomic cloning and chromosomal assignment of rat regucalcin gene. Mol Cell Biochem 151(2):157–163PubMedCrossRefGoogle Scholar
  9. 9.
    Yamaguchi M, Makino R, Shimokawa N (1996) The 5′ end sequences and exon organization in rat regucalcin gene. Mol Cell Biochem 165(2):145–150PubMedCrossRefGoogle Scholar
  10. 10.
    Fujita T, Shirasawa T, Maruyama N (1996) Isolation and characterization of genomic and cDNA clones encoding mouse senescence marker protein-30 (SMP30). Biochim Biophys Acta 1308(1):49–57PubMedCrossRefGoogle Scholar
  11. 11.
    Maia C, Santos C, Schmitt F, Socorro S (2009) Regucalcin is under-expressed in human breast and prostate cancers: effect of sex steroid hormones. J Cell Biochem 107(4):667–676PubMedCrossRefGoogle Scholar
  12. 12.
    Fujita T, Shirasawa T, Uchida K, Maruyama N (1992) Isolation of cDNA clone encoding rat senescence marker protein-30 (SMP30) and its tissue distribution. Biochim Biophys Acta 1132(3):297–305PubMedCrossRefGoogle Scholar
  13. 13.
    Fujita T, Uchida K, Maruyama N (1992) Purification of senescence marker protein-30 (SMP30) and its androgen-independent decrease with age in the rat liver. Biochim Biophys Acta 1116(2):122–128PubMedCrossRefGoogle Scholar
  14. 14.
    Fujita T, Shirasawa T, Uchida K, Maruyama N (1996) Gene regulation of senescence marker protein-30 (SMP30): coordinated up-regulation with tissue maturation and gradual down-regulation with aging. Mech Ageing Dev 87(3):219–229PubMedCrossRefGoogle Scholar
  15. 15.
    Shimokawa N, Yamaguchi M (1992) Calcium administration stimulates the expression of calcium-binding protein regucalcin mRNA in rat liver. FEBS Lett 305(2):151–154PubMedCrossRefGoogle Scholar
  16. 16.
    Yamaguchi M, Isogai M (1993) Tissue concentration of calcium-binding protein regucalcin in rats by enzyme-linked immunoadsorbent assay. Mol Cell Biochem 122(1):65–68PubMedCrossRefGoogle Scholar
  17. 17.
    Yamaguchi M, Isogai M, Kato S, Mori S (1991) Immunohistochemical demonstration of calcium-binding protein regucalcin in the tissues of rats: the protein localizes in liver and brain. Chem Pharm Bull (Tokyo) 39(6):1601–1603CrossRefGoogle Scholar
  18. 18.
    Shimokawa N, Isogai M, Yamaguchi M (1995) Specific species and tissue differences for the gene expression of calcium-binding protein regucalcin. Mol Cell Biochem 143(1):67–71PubMedCrossRefGoogle Scholar
  19. 19.
    Misawa H, Yamaguchi M (2000) The gene of Ca2 + -binding protein regucalcin is highly conserved in vertebrate species. Int J Mol Med 6(2):191–196PubMedGoogle Scholar
  20. 20.
    Goto SG (2000) Expression of Drosophila homologue of senescence marker protein-30 during cold acclimation. J Insect Physiol 46(7):1111–1120PubMedCrossRefGoogle Scholar
  21. 21.
    Yamaguchi M (2011) The transcriptional regulation of regucalcin gene expression. Mol Cell Biochem 346(1–2):147–171PubMedCrossRefGoogle Scholar
  22. 22.
    Yamaguchi M, Kurota H (1995) Expression of calcium-binding protein regucalcin mRNA in the kidney cortex of rats: the stimulation by calcium administration. Mol Cell Biochem 146(1):71–77PubMedCrossRefGoogle Scholar
  23. 23.
    Shimokawa N, Yamaguchi M (1993) Expression of hepatic calcium-binding protein regucalcin mRNA is mediated through Ca2 +/calmodulin in rat liver. FEBS Lett 316(1):79–84PubMedCrossRefGoogle Scholar
  24. 24.
    Nakajima M, Murata T, Yamaguchi M (1999) Expression of calcium-binding protein regucalcin mRNA in the cloned rat hepatoma cells (H4-II-E) is stimulated through Ca2 + signaling factors: involvement of protein kinase C. Mol Cell Biochem 198(1–2):101–107PubMedCrossRefGoogle Scholar
  25. 25.
    Yamaguchi M, Nakajima M (1999) Involvement of intracellular signaling factors in the serum-enhanced Ca2 + -binding protein regucalcin mRNA expression in the cloned rat hepatoma cells (H4-II-E). J Cell Biochem 74(1):81–89PubMedCrossRefGoogle Scholar
  26. 26.
    Maia CJ, Santos CR, Schmitt F, Socorro S (2008) Regucalcin is expressed in rat mammary gland and prostate and down-regulated by 17beta-estradiol. Mol Cell Biochem 311(1–2):81–86PubMedCrossRefGoogle Scholar
  27. 27.
    Kurota H, Yamaguchi M (1996) Steroid hormonal regulation of calcium-binding protein regucalcin mRNA expression in the kidney cortex of rats. Mol Cell Biochem 155(2):105–111PubMedCrossRefGoogle Scholar
  28. 28.
    Sar P, Rath B, Subudhi U, Chainy GB, Supakar PC (2007) Alterations in expression of senescence marker protein-30 gene by 3,3′,5-triiodo-L-thyronine (T3). Mol Cell Biochem 303(1–2):239–242PubMedCrossRefGoogle Scholar
  29. 29.
    Yamaguchi M, Kanayama Y, Shimokawa N (1994) Expression of calcium-binding protein regucalcin mRNA in rat liver is stimulated by calcitonin: the hormonal effect is mediated through calcium. Mol Cell Biochem 136(1):43–48PubMedCrossRefGoogle Scholar
  30. 30.
    Nakagawa T, Yamaguchi M (2008) Nuclear localization of regucalcin is enhanced in culture with protein kinase C activation in cloned normal rat kidney proximal tubular epithelial NRK52E cells. Int J Mol Med 21(5):605–610PubMedGoogle Scholar
  31. 31.
    Kim HS, Son TG, Park HR, Lee Y, Jung Y, Ishigami A, Lee J (2012) Senescence marker protein 30 deficiency increases Parkinson’s pathology by impairing astrocyte activation. Neurobiol Aging. doi: 10.1016/j.neurobiolaging.2012.10.008 Google Scholar
  32. 32.
    Son TG, Park HR, Kim SJ, Kim K, Kim MS, Ishigami A, Handa S, Maruyama N, Chung HY, Lee J (2009) Senescence marker protein 30 is up-regulated in kainate-induced hippocampal damage through ERK-mediated astrocytosis. J Neurosci Res 87(13):2890–2897PubMedCrossRefGoogle Scholar
  33. 33.
    Sun L, Wang L, Sun Y, Tang SW, Hu Y (2006) Protective effects of EUK4010 on beta-amyloid(1–42) induced degeneration of neuronal cells. Eur J Neurosci 24(4):1011–1019PubMedCrossRefGoogle Scholar
  34. 34.
    Laurentino SS, Correia S, Cavaco JE, Oliveira PF, de Sousa M, Barros A, Socorro S (2012) Regucalcin, a calcium-binding protein with a role in male reproduction? Mol Hum Reprod 18(4):161–170PubMedCrossRefGoogle Scholar
  35. 35.
    Lv S, Wang JH, Liu F, Gao Y, Fei R, Du SC, Wei L (2008) Senescence marker protein 30 in acute liver failure: validation of a mass spectrometry proteomics assay. BMC Gastroenterol 8:17PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Yamaguchi M, Tsurusaki Y, Misawa H, Inagaki S, Ma ZJ, Takahashi H (2002) Potential role of regucalcin as a specific biochemical marker of chronic liver injury with carbon tetrachloride administration in rats. Mol Cell Biochem 241(1–2):61–67PubMedCrossRefGoogle Scholar
  37. 37.
    Zhou SF, Mo FR, Bin YH, Hou GQ, Xie XX, Luo GR (2011) Serum immunoreactivity of SMP30 and its tissues expression in hepatocellular carcinoma. Clin Biochem 44(4):331–336PubMedCrossRefGoogle Scholar
  38. 38.
    Doran P, Dowling P, Donoghue P, Buffini M, Ohlendieck K (2006) Reduced expression of regucalcin in young and aged mdx diaphragm indicates abnormal cytosolic calcium handling in dystrophin-deficient muscle. Biochim Biophys Acta 1764(4):773–785PubMedCrossRefGoogle Scholar
  39. 39.
    Park H, Ishigami A, Shima T, Mizuno M, Maruyama N, Yamaguchi K, Mitsuyoshi H, Minami M, Yasui K, Itoh Y, Yoshikawa T, Fukui M, Hasegawa G, Nakamura N, Ohta M, Obayashi H, Okanoue T (2009) Hepatic senescence marker protein-30 is involved in the progression of nonalcoholic fatty liver disease. J Gastroenterol 45(4):426–434PubMedCrossRefGoogle Scholar
  40. 40.
    Tsurusaki Y, Misawa H, Yamaguchi M (2000) Translocation of regucalcin to rat liver nucleus: involvement of nuclear protein kinase and protein phosphatase regulation. Int J Mol Med 6(6):655–660PubMedGoogle Scholar
  41. 41.
    Ishigami A, Handa S, Maruyama N, Supakar PC (2003) Nuclear localization of senescence marker protein-30, SMP30, in cultured mouse hepatocytes and its similarity to RNA polymerase. Biosci Biotechnol Biochem 67(1):158–160PubMedCrossRefGoogle Scholar
  42. 42.
    Arun P, Aleti V, Parikh K, Manne V, Chilukuri N (2011) Senescence Marker Protein 30 (SMP30) Expression in Eukaryotic Cells: existence of Multiple Species and Membrane Localization. PLoS ONE 6(2):e16545PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Yamaguchi M (2005) Role of regucalcin in maintaining cell homeostasis and function (review). Int J Mol Med 15(3):371–389PubMedGoogle Scholar
  44. 44.
    Yamaguchi M (2012) Role of regucalcin in brain calcium signaling: involvement in aging. Integr Biol (Camb) 4(8):825–837CrossRefGoogle Scholar
  45. 45.
    Baba T, Yamaguchi M (2000) Stimulatory effect of regucalcin on proteolytic activity is impaired in the kidney cortex cytosol of rats with saline ingestion. Mol Cell Biochem 206(1–2):1–6PubMedCrossRefGoogle Scholar
  46. 46.
    Katsumata T, Yamaguchi M (1998) Inhibitory effect of calcium-binding protein regucalcin on protein kinase activity in the nuclei of regenerating rat liver. J Cell Biochem 71(4):569–576PubMedCrossRefGoogle Scholar
  47. 47.
    Fukaya Y, Yamaguchi M (2004) Characterization of protein tyrosine phosphatase activity in rat liver microsomes: suppressive effect of endogenous regucalcin in transgenic rats. Int J Mol Med 14(3):427–432PubMedGoogle Scholar
  48. 48.
    Tobisawa M, Yamaguchi M (2003) Inhibitory role of regucalcin in the regulation of nitric oxide synthase activity in rat brain cytosol: involvement of aging. J Neurol Sci 209(1–2):47–54PubMedCrossRefGoogle Scholar
  49. 49.
    Son TG, Kim SJ, Kim K, Kim MS, Chung HY, Lee J (2008) Cytoprotective roles of senescence marker protein 30 against intracellular calcium elevation and oxidative stress. Arch Pharm Res 31(7):872–877PubMedCrossRefGoogle Scholar
  50. 50.
    Fukaya Y, Yamaguchi M (2004) Regucalcin increases superoxide dismutase activity in rat liver cytosol. Biol Pharm Bull 27(9):1444–1446PubMedCrossRefGoogle Scholar
  51. 51.
    Handa S, Maruyama N, Ishigami A (2009) Over-expression of Senescence Marker Protein-30 decreases reactive oxygen species in human hepatic carcinoma Hep G2 cells. Biol Pharm Bull 32(10):1645–1648PubMedCrossRefGoogle Scholar
  52. 52.
    Ichikawa E, Yamaguchi M (2004) Regucalcin increases superoxide dismutase activity in the heart cytosol of normal and regucalcin transgenic rats. Int J Mol Med 14(4):691–695PubMedGoogle Scholar
  53. 53.
    Tsurusaki Y, Yamaguchi M (2003) Overexpression of regucalcin modulates tumor-related gene expression in cloned rat hepatoma H4-II-E cells. J Cell Biochem 90(3):619–626PubMedCrossRefGoogle Scholar
  54. 54.
    Yamaguchi M, Daimon Y (2005) Overexpression of regucalcin suppresses cell proliferation in cloned rat hepatoma H4-II-E cells: involvement of intracellular signaling factors and cell cycle-related genes. J Cell Biochem 95(6):1169–1177PubMedCrossRefGoogle Scholar
  55. 55.
    Misawa H, Inagaki S, Yamaguchi M (2002) Suppression of cell proliferation and deoxyribonucleic acid synthesis in the cloned rat hepatoma H4-II-E cells overexpressing regucalcin. J Cell Biochem 84(1):143–149CrossRefGoogle Scholar
  56. 56.
    Izumi T, Yamaguchi M (2004) Overexpression of regucalcin suppresses cell death in cloned rat hepatoma H4-II-E cells induced by tumor necrosis factor-alpha or thapsigargin. J Cell Biochem 92(2):296–306PubMedCrossRefGoogle Scholar
  57. 57.
    Nakagawa T, Sawada N, Yamaguchi M (2005) Overexpression of regucalcin suppresses cell proliferation of cloned normal rat kidney proximal tubular epithelial NRK52E cells. Int J Mol Med 16(4):637–643PubMedGoogle Scholar
  58. 58.
    Matsuyama S, Kitamura T, Enomoto N, Fujita T, Ishigami A, Handa S, Maruyama N, Zheng D, Ikejima K, Takei Y, Sato N (2004) Senescence marker protein-30 regulates Akt activity and contributes to cell survival in Hep G2 cells. Biochem Biophys Res Commun 321(2):386–390PubMedCrossRefGoogle Scholar
  59. 59.
    Jeong DH, Goo MJ, Hong IH, Yang HJ, Ki MR, Do SH, Ha JH, Lee SS, Park JK, Jeong KS (2008) Inhibition of radiation-induced apoptosis via overexpression of SMP30 in Smad3-knockout mice liver. J Radiat Res (Tokyo) 49(6):653–660CrossRefGoogle Scholar
  60. 60.
    Ishigami A, Fujita T, Handa S, Shirasawa T, Koseki H, Kitamura T, Enomoto N, Sato N, Shimosawa T, Maruyama N (2002) Senescence marker protein-30 knockout mouse liver is highly susceptible to tumor necrosis factor-alpha- and Fas-mediated apoptosis. Am J Pathol 161(4):1273–1281PubMedCrossRefGoogle Scholar
  61. 61.
    Maruyama N, Ishigami A, Kondo Y (2010) Pathophysiological significance of senescence marker protein-30. Geriatr Gerontol Int 10(Suppl 1):S88–S98PubMedCrossRefGoogle Scholar
  62. 62.
    Nikapitiya C, De Zoysa M, Kang HS, Oh C, Whang I, Lee J (2008) Molecular characterization and expression analysis of regucalcin in disk abalone (Haliotis discus discus): intramuscular calcium administration stimulates the regucalcin mRNA expression. Comp Biochem Physiol B 150(1):117–124PubMedCrossRefGoogle Scholar
  63. 63.
    Wu YD, Jiang L, Zhou Z, Zheng MH, Zhang J, Liang Y (2008) CYP1A/regucalcin gene expression and edema formation in zebrafish embryos exposed to 2,3,7,8-Tetrachlorodibenzo-p-dioxin. Bull Environ Contam Toxicol 80(6):482–486PubMedCrossRefGoogle Scholar
  64. 64.
    Nakajima Y, Natori S (2000) Identification and characterization of an anterior fat body protein in an insect. J Biochem 127(5):901–908PubMedCrossRefGoogle Scholar
  65. 65.
    Gomi K, Hirokawa K, Kajiyama N (2002) Molecular cloning and expression of the cDNAs encoding luciferin-regenerating enzyme from Luciola cruciata and Luciola lateralis. Gene 294(1–2):157–166PubMedCrossRefGoogle Scholar
  66. 66.
    Laurentino SS, Correia S, Cavaco JE, Oliveira PF, Rato L, Sousa M, Barros A, Socorro S (2011) Regucalcin is broadly expressed in male reproductive tissues and is a new androgen-target gene in mammalian testis. Reproduction 142(3):447–456PubMedCrossRefGoogle Scholar
  67. 67.
    Nakagawa T, Yamaguchi M (2005) Hormonal regulation on regucalcin mRNA expression in cloned normal rat kidney proximal tubular epithelial NRK52E cells. J Cell Biochem 95(3):589–597PubMedCrossRefGoogle Scholar
  68. 68.
    Jung KJ, Maruyama N, Ishigami A, Yu BP, Chung HY (2006) The redox-sensitive DNA binding sites responsible for age-related downregulation of SMP30 by ERK pathway and reversal by calorie restriction. Antioxid Redox Signal 8(3–4):671–680PubMedCrossRefGoogle Scholar
  69. 69.
    Fujita T, Maruyama N (1998) Expression and structure of senescence marker protein-30 (SMP30) and its physiological function. Nippon Ronen Igakkai Zasshi 35(9):654–657PubMedCrossRefGoogle Scholar
  70. 70.
    Yamaguchi M, Misawa H, Uchiyama S, Morooka Y, Tsurusaki Y (2002) Role of endogenous regucalcin in bone metabolism: bone loss is induced in regucalcin transgenic rats. Int J Mol Med 10(4):377–383PubMedGoogle Scholar
  71. 71.
    Yamaguchi M, Morooka Y, Misawa H, Tsurusaki Y, Nakajima R (2002) Role of endogenous regucalcin in transgenic rats: suppression of kidney cortex cytosolic protein phosphatase activity and enhancement of heart muscle microsomal Ca2 + -ATPase activity. J Cell Biochem 86(3):520–529PubMedCrossRefGoogle Scholar
  72. 72.
    Yamaguchi M, Sawada N, Uchiyama S, Misawa H, Ma ZJ (2004) Expression of regucalcin in rat bone marrow cells: involvement of osteoclastic bone resorption in regucalcin transgenic rats. Int J Mol Med 13(3):437–443PubMedGoogle Scholar
  73. 73.
    Ishii K, Tsubaki T, Fujita K, Ishigami A, Maruyama N, Akita M (2005) Immunohistochemical localization of senescence marker protein-30 (SMP30) in the submandibular gland and ultrastructural changes of the granular duct cells in SMP30 knockout mice. Histol Histopathol 20(3):761–768PubMedGoogle Scholar
  74. 74.
    Yamaguchi M, Nakajima R (2002) Role of regucalcin as an activator of sarcoplasmic reticulum Ca2 + -ATPase activity in rat heart muscle. J Cell Biochem 86(1):184–193PubMedCrossRefGoogle Scholar
  75. 75.
    van Dijk KD, Berendse HW, Drukarch B, Fratantoni SA, Pham TV, Piersma SR, Huisman E, Breve JJ, Groenewegen HJ, Jimenez CR, van de Berg WD (2012) The proteome of the locus ceruleus in Parkinson’s disease: relevance to pathogenesis. Brain Pathol 22(4):485–498PubMedCrossRefGoogle Scholar
  76. 76.
    Isogai M, Shimokawa N, Yamaguchi M (1994) Hepatic calcium-binding protein regucalcin in released into the serum of rats administered orally carbon tetrachloride. Mol Cell Biochem 131(2):173–179PubMedCrossRefGoogle Scholar
  77. 77.
    Isogai M, Oishi K, Yamaguchi M (1994) Serum release of hepatic calcium-binding protein regucalcin by liver injury with galactosamine administration in rats. Mol Cell Biochem 136(1):85–90PubMedCrossRefGoogle Scholar
  78. 78.
    Lv S, Wei L, Wang JH, Wang JY, Liu F (2007) Identification of novel molecular candidates for acute liver failure in plasma of BALB/c murine model. J Proteome Res 6(7):2746–2752PubMedCrossRefGoogle Scholar
  79. 79.
    Carolan JC, Fitzroy CI, Ashton PD, Douglas AE, Wilkinson TL (2009) The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9(9):2457–2467PubMedCrossRefGoogle Scholar
  80. 80.
    Inoue H, Fujita T, Kitamura T, Shimosawa T, Nagasawa R, Inoue R, Maruyama N, Nagasawa T (1999) Senescence marker protein-30 (SMP30) enhances the calcium efflux from renal tubular epithelial cells. Clin Exp Nephrol 3(4):261–267CrossRefGoogle Scholar
  81. 81.
    Ueoka S, Yamaguchi M (1998) Sexual difference of hepatic calcium-binding protein regucalcin mRNA expression in rats with different ages: effect of ovarian hormone. Biol Pharm Bull 21(4):405–407PubMedCrossRefGoogle Scholar
  82. 82.
    Murata T, Yamaguchi M (1997) Molecular cloning of the cDNA coding for regucalcin and its mRNA expression in mouse liver: the expression is stimulated by calcium administration. Mol Cell Biochem 173(1–2):127–133PubMedCrossRefGoogle Scholar
  83. 83.
    Fujita T, Shirasawa T, Maruyama N (1999) Expression and structure of senescence marker protein-30 (SMP30) and its biological significance. Mech Ageing Dev 107(3):271–280PubMedCrossRefGoogle Scholar
  84. 84.
    Makino R, Yamaguchi M (1996) Expression of calcium-binding protein regucalcin mRNA in hepatoma cells. Mol Cell Biochem 155(1):85–90PubMedCrossRefGoogle Scholar
  85. 85.
    Yamaguchi M (1998) Role of calcium-binding protein regucalcin in regenerating rat liver. J Gastroenterol Hepatol 13(Suppl):S106–S112PubMedGoogle Scholar
  86. 86.
    Murata T, Yamaguchi M (1998) Ca2 + administration stimulates the binding of AP-1 factor to the 5′-flanking region of the rat gene for the Ca2 + -binding protein regucalcin. Biochem J 329(Pt 1):157–163PubMedGoogle Scholar
  87. 87.
    Inagaki S, Misawa H, Yamaguchi M (2000) Role of endogenous regucalcin in protein tyrosine phosphatase regulation in the cloned rat hepatoma cells (H4-II-E). Mol Cell Biochem 213(1–2):43–50PubMedCrossRefGoogle Scholar
  88. 88.
    Ishigami A, Fujita T, Inoue H, Handa S, Kubo S, Kondo Y, Maruyama N (2005) Senescence marker protein-30 (SMP30) induces formation of microvilli and bile canaliculi in Hep G2 cells. Cell Tissue Res 320(2):243–249PubMedCrossRefGoogle Scholar
  89. 89.
    Fujita T, Inoue H, Kitamura T, Sato N, Shimosawa T, Maruyama N (1998) Senescence marker protein-30 (SMP30) rescues cell death by enhancing plasma membrane Ca(2 +)-pumping activity in Hep G2 cells. Biochem Biophys Res Commun 250(2):374–380PubMedCrossRefGoogle Scholar
  90. 90.
    Murata T, Shinya N, Yamaguchi M (1997) Expression of calcium-binding protein regucalcin mRNA in the cloned human hepatoma cells (HepG2): stimulation by insulin. Mol Cell Biochem 175(1–2):163–168PubMedCrossRefGoogle Scholar
  91. 91.
    Misawa H, Yamaguchi M (2000) Transcript heterogeneity of the human gene for Ca2 + -binding protein regucalcin. Int J Mol Med 5(3):283–287PubMedGoogle Scholar
  92. 92.
    Yamaguchi M, Kobayashi M, Uchiyama S (2005) Suppressive effect of regucalcin on cell differentiation and mineralization in osteoblastic MC3T3-E1 cells. J Cell Biochem 96(3):543–554PubMedCrossRefGoogle Scholar
  93. 93.
    Suzuki S, Asamoto M, Tsujimura K, Shirai T (2004) Specific differences in gene expression profile revealed by cDNA microarray analysis of glutathione S-transferase placental form (GST-P) immunohistochemically positive rat liver foci and surrounding tissue. Carcinogenesis 25(3):439–443PubMedCrossRefGoogle Scholar
  94. 94.
    Yamaguchi M, Isogai M, Shimada N (1997) Potential sensitivity of hepatic specific protein regucalcin as a marker of chronic liver injury. Mol Cell Biochem 167(1–2):187–190PubMedCrossRefGoogle Scholar
  95. 95.
    Yamaguchi M, Oishi K, Isogai M (1995) Expression of hepatic calcium-binding protein regucalcin mRNA is elevated by refeeding of fasted rats: involvement of glucose, insulin and calcium as stimulating factors. Mol Cell Biochem 142(1):35–41PubMedCrossRefGoogle Scholar
  96. 96.
    Shinya N, Yamaguchi M (1998) Stimulatory effect of calcium administration on regucalcin mRNA expression is attenuated in the kidney cortex of rats ingested with saline. Mol Cell Biochem 178(1–2):275–281PubMedCrossRefGoogle Scholar
  97. 97.
    Ramasamy I (2006) Recent advances in physiological calcium homeostasis. Clin Chem Lab Med 44(3):237–273PubMedCrossRefGoogle Scholar
  98. 98.
    Yamaguchi M (2010) Regucalcin and metabolic disorders: osteoporosis and hyperlipidemia are induced in regucalcin transgenic rats. Mol Cell Biochem 341(1–2):119–133PubMedCrossRefGoogle Scholar
  99. 99.
    Yamaguchi M, Otomo Y, Uchiyama S, Nakagawa T (2008) Hormonal regulation of regucalcin mRNA expression in osteoblastic MC3T3-E1 cells. Int J Mol Med 21(6):771–775PubMedGoogle Scholar
  100. 100.
    Yamaguchi M, Weitzmann MN, Murata T (2012) Exogenous regucalcin stimulates osteoclastogenesis and suppresses osteoblastogenesis through NF-kappaB activation. Mol Cell Biochem 359(1–2):193–203PubMedCrossRefGoogle Scholar
  101. 101.
    Yamaguchi M, Oishi K (1995) 17 beta-Estradiol stimulates the expression of hepatic calcium-binding protein regucalcin mRNA in rats. Mol Cell Biochem 143(2):137–141PubMedCrossRefGoogle Scholar
  102. 102.
    Sar P, Peter R, Rath B, Mohapatra AD, Mishra SK (2011) 3, 3′5 Triiodo L Thyronine Induces Apoptosis in Human Breast Cancer MCF-7cells, Repressing SMP30 Expression through Negative Thyroid Response Elements. PLoS ONE 6(6):e20861PubMedCentralPubMedCrossRefGoogle Scholar
  103. 103.
    Shinya N, Kurota H, Yamaguchi M (1996) Calcium-binding protein regucalcin mRNA expression in the kidney cortex is suppressed by saline ingestion in rats. Mol Cell Biochem 162(2):139–144PubMedCrossRefGoogle Scholar
  104. 104.
    Fukui M, Senmaru T, Hasegawa G, Yamazaki M, Asano M, Kagami Y, Ishigami A, Maruyama N, Iwasa K, Kitawaki J, Itoh Y, Okanoue T, Ohta M, Obayashi H, Nakamura N (2011) 17beta-Estradiol attenuates saturated fatty acid diet-induced liver injury in ovariectomized mice by up-regulating hepatic senescence marker protein-30. Biochem Biophys Res Commun 415(2):252–257PubMedCrossRefGoogle Scholar
  105. 105.
    Speakman JR, Mitchell SE (2011) Caloric restriction. Mol Aspects Med 32(3):159–221PubMedCrossRefGoogle Scholar
  106. 106.
    Jung KJ, Ishigami A, Maruyama N, Takahashi R, Goto S, Yu BP, Chung HY (2004) Modulation of gene expression of SMP-30 by LPS and calorie restriction during aging process. Exp Gerontol 39(8):1169–1177PubMedCrossRefGoogle Scholar
  107. 107.
    Ishigami T, Fujita T, Simbula G, Columbano A, Kikuchi K, Ishigami A, Shimosawa T, Arakawa Y, Maruyama N (2001) Regulatory effects of senescence marker protein 30 on the proliferation of hepatocytes. Pathol Int 51(7):491–497PubMedCrossRefGoogle Scholar
  108. 108.
    Lee WJ, Monteith GR, Roberts-Thomson SJ (2006) Calcium transport and signaling in the mammary gland: targets for breast cancer. BBA Rev Cancer 1765(2):235–255Google Scholar
  109. 109.
    Cheng HP, Wei S, Wei LP, Verkhratsky A (2006) Calcium signaling in physiology and pathophysiology. Acta Pharmacol Sin 27(7):767–772PubMedCrossRefGoogle Scholar
  110. 110.
    Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4(7):517–529PubMedCrossRefGoogle Scholar
  111. 111.
    Birnbaumer L (2009) The TRPC class of ion channels: a critical review of their roles in slow, sustained increases in intracellular Ca(2 +) concentrations. Annu Rev Pharmacol Toxicol 49:395–426PubMedCrossRefGoogle Scholar
  112. 112.
    Nakagawa T, Yamaguchi M (2006) Overexpression of regucalcin enhances its nuclear localization and suppresses L-type Ca2 + channel and calcium-sensing receptor mRNA expressions in cloned normal rat kidney proximal tubular epithelial NRK52E cells. J Cell Biochem 99(4):1064–1077PubMedCrossRefGoogle Scholar
  113. 113.
    Yamaguchi M, Mori S, Kato S (1988) Calcium-binding protein regucalcin is an activator of (Ca2 + -Mg2 +)-adenosine triphosphatase in the plasma membranes of rat liver. Chem Pharm Bull (Tokyo) 36(9):3532–3539CrossRefGoogle Scholar
  114. 114.
    Takahashi H, Yamaguchi M (1993) Regucalcin modulates hormonal effect on (Ca(2 +)-Mg2 +)-ATPase activity in rat liver plasma membranes. Mol Cell Biochem 125(2):171–177PubMedCrossRefGoogle Scholar
  115. 115.
    Takahashi H, Yamaguchi M (1997) Stimulatory effect of regucalcin on ATP-dependent calcium transport in rat liver plasma membranes. Mol Cell Biochem 168(1–2):149–153PubMedCrossRefGoogle Scholar
  116. 116.
    Takahashi H, Yamaguchi M (1994) Activating effect of regucalcin on (Ca(2 +)-Mg2 +)-ATPase in rat liver plasma membranes: relation to sulfhydryl group. Mol Cell Biochem 136(1):71–76PubMedCrossRefGoogle Scholar
  117. 117.
    Takahasi H, Yamaguchi M (1996) Enhancement of plasma membrane (Ca(2 +)-Mg2 +)-ATPase activity in regenerating rat liver: involvement of endogenous activating protein regucalcin. Mol Cell Biochem 162(2):133–138PubMedCrossRefGoogle Scholar
  118. 118.
    Takahashi H, Yamaguchi M (1995) Increase of (Ca(2 +)-Mg2 +)-ATPase activity in hepatic plasma membranes of rats administered orally calcium: the endogenous role of regucalcin. Mol Cell Biochem 144(1):1–6PubMedCrossRefGoogle Scholar
  119. 119.
    Di Leva F, Domi T, Fedrizzi L, Lim D, Carafoli E (2008) The plasma membrane Ca2 + ATPase of animal cells: structure, function and regulation. Arch Biochem Biophys 476(1):65–74PubMedCrossRefGoogle Scholar
  120. 120.
    Takahashi H, Yamaguchi M (1996) Activatory effect of regucalcin on hepatic plasma membrane (Ca(2 +)-Mg2 +)-ATPase is impaired by liver injury with carbon tetrachloride administration in rats. Mol Cell Biochem 158(1):9–16PubMedGoogle Scholar
  121. 121.
    Kurota H, Yamaguchi M (1997) Activatory effect of calcium-binding protein regucalcin on ATP-dependent calcium transport in the basolateral membranes of rat kidney cortex. Mol Cell Biochem 169(1–2):149–156PubMedCrossRefGoogle Scholar
  122. 122.
    Yamaguchi M, Mori S (1989) Activation of hepatic microsomal Ca2 + -adenosine triphosphatase by calcium-binding protein regucalcin. Chem Pharm Bull (Tokyo) 37(4):1031–1034CrossRefGoogle Scholar
  123. 123.
    Takahashi H, Yamaguchi M (1999) Role of regucalcin as an activator of Ca(2 +)-ATPase activity in rat liver microsomes. J Cell Biochem 74(4):663–669PubMedCrossRefGoogle Scholar
  124. 124.
    Lai P, Yip NC, Michelangeli F (2011) Regucalcin (RGN/SMP30) alters agonist- and thapsigargin-induced cytosolic [Ca(2 +)] transients in cells by increasing SERCA Ca(2 +)ATPase levels. FEBS Lett 585(14):2291–2294PubMedCrossRefGoogle Scholar
  125. 125.
    Yamaguchi M, Hanahisa Y, Murata T (1999) Expression of calcium-binding protein regucalcin and microsomal Ca2 + -ATPase regulation in rat brain: attenuation with increasing age. Mol Cell Biochem 200(1–2):43–49PubMedCrossRefGoogle Scholar
  126. 126.
    Omura M, Yamaguchi M (1999) Regulation of protein phosphatase activity by regucalcin localization in rat liver nuclei. J Cell Biochem 75(3):437–445PubMedCrossRefGoogle Scholar
  127. 127.
    Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89(4):1341–1378PubMedCrossRefGoogle Scholar
  128. 128.
    Yamaguchi M (1992) Effect of calcium-binding protein regucalcin on Ca2 + transport system in rat liver nuclei: stimulation of Ca2 + release. Mol Cell Biochem 113(1):63–70PubMedCrossRefGoogle Scholar
  129. 129.
    Tsurusaki Y, Yamaguchi M (2000) Role of endogenous regucalcin in the regulation of Ca(2 +)-ATPase activity in rat liver nuclei. J Cell Biochem 78(4):541–549PubMedCrossRefGoogle Scholar
  130. 130.
    Mori S, Yamaguchi M (1991) Calcium-binding protein regucalcin stimulates the uptake of Ca2 + by rat liver mitochondria. Chem Pharm Bull (Tokyo) 39(1):224–226CrossRefGoogle Scholar
  131. 131.
    Takahashi H, Yamaguchi M (2000) Stimulatory effect of regucalcin on ATP-dependent Ca(2 +) uptake activity in rat liver mitochondria. J Cell Biochem 78(1):121–130PubMedCrossRefGoogle Scholar
  132. 132.
    Xue JH, Takahashi H, Yamaguchi M (2000) Stimulatory effect of regucalcin on mitochondrial ATP-dependent calcium uptake activity in rat kidney cortex. J Cell Biochem 80(2):285–292PubMedCrossRefGoogle Scholar
  133. 133.
    Akhter T, Sawada N, Yamaguchi M (2006) Regucalcin increases Ca2 + -ATPase activity in the heart mitochondria of normal and regucalcin transgenic rats. Int J Mol Med 18(1):171–176PubMedGoogle Scholar
  134. 134.
    Yamaguchi M, Takakura Y, Nakagawa T (2008) Regucalcin increases Ca2 + -ATPase activity in the mitochondria of brain tissues of normal and transgenic rats. J Cell Biochem 104(3):795–804PubMedCrossRefGoogle Scholar
  135. 135.
    Yamaguchi M, Mori S (1988) Effect of Ca2 + and Zn2 + on 5′-nucleotidase activity in rat liver plasma membranes: hepatic calcium-binding protein (regucalcin) reverses the Ca2 + effect. Chem Pharm Bull (Tokyo) 36(1):321–325CrossRefGoogle Scholar
  136. 136.
    Yamaguchi M, Shibano H (1987) Reversible effect of calcium-binding protein on the Ca2 + -induced activation of succinate dehydrogenase in rat liver mitochondria. Chem Pharm Bull (Tokyo) 35(9):3700–3766Google Scholar
  137. 137.
    Yamaguchi M, Shibano H (1987) Effect of calcium-binding protein on the activation of phosphorylase a in rat hepatic particulate glycogen by Ca2+. Chem Pharm Bull (Tokyo) 35(6):2581–2584CrossRefGoogle Scholar
  138. 138.
    Yamaguchi M, Shibano H (1987) Calcium-binding protein isolated from rat liver cytosol reverses activation of pyruvate kinase by Ca2+. Chem Pharm Bull (Tokyo) 35(5):2025–2029CrossRefGoogle Scholar
  139. 139.
    Yamaguchi M, Mori S, Suketa Y (1989) Effects of Ca2 + and V5 + on glucose-6-phosphatase activity in rat liver microsomes: the Ca2 + effect is reversed by regucalcin. Chem Pharm Bull (Tokyo) 37(2):388–390CrossRefGoogle Scholar
  140. 140.
    Hanahisa Y, Yamaguchi M (1999) Effect of calcium-binding protein on adenosine 5′-triphosphatase activity in the brain cytosol of rats of different ages: the inhibitory role of regucalcin. Biol Pharm Bull 22(3):313–316PubMedCrossRefGoogle Scholar
  141. 141.
    Yamaguchi M, Yoshida H (1985) Regulatory effect of calcium-binding protein isolated from rat liver cytosol on activation of fructose 1,6-diphosphatase by Ca2 + -calmodulin. Chem Pharm Bull (Tokyo) 33(10):4489–4493CrossRefGoogle Scholar
  142. 142.
    Yamaguchi M, Sakurai T (1992) Reversible effect of calcium-binding protein regucalcin on the Ca(2 +)-induced inhibition of deoxyuridine 5′-triphosphatase activity in rat liver cytosol. Mol Cell Biochem 110(1):25–29PubMedCrossRefGoogle Scholar
  143. 143.
    Halls ML, Cooper DM (2011) Regulation by Ca2 + -signaling pathways of adenylyl cyclases. Cold Spring Harb Perspect Biol 3(1):a004143PubMedCrossRefGoogle Scholar
  144. 144.
    Tresguerres M, Levin LR, Buck J (2011) Intracellular cAMP signaling by soluble adenylyl cyclase. Kidney Int 79(12):1277–1288PubMedCentralPubMedCrossRefGoogle Scholar
  145. 145.
    Levy I, Horvath A, Azevedo M, de Alexandre RB, Stratakis CA (2011) Phosphodiesterase function and endocrine cells: links to human disease and roles in tumor development and treatment. Curr Opin Pharmacol 11(6):689–697PubMedCrossRefGoogle Scholar
  146. 146.
    Yamaguchi M, Tai H (1991) Inhibitory effect of calcium-binding protein regucalcin on Ca2 +/calmodulin-dependent cyclic nucleotide phosphodiesterase activity in rat liver cytosol. Mol Cell Biochem 106(1):25–30PubMedCrossRefGoogle Scholar
  147. 147.
    Yamaguchi M, Kurota H (1997) Inhibitory effect of regucalcin on Ca2 +/calmodulin-dependent cyclic AMP phosphodiesterase activity in rat kidney cytosol. Mol Cell Biochem 177(1–2):209–214PubMedCrossRefGoogle Scholar
  148. 148.
    Daff S (2010) NO synthase: structures and mechanisms. Nitric Oxide 23(1):1–11PubMedCrossRefGoogle Scholar
  149. 149.
    Ma ZJ, Yamaguchi M (2003) Regulatory effect of regucalcin on nitric oxide synthase activity in rat kidney cortex cytosol: role of endogenous regucalcin in transgenic rats. Int J Mol Med 12(2):201–206PubMedGoogle Scholar
  150. 150.
    Yamaguchi M, Takahashi H, Tsurusaki Y (2003) Suppressive role of endogenous regucalcin in the enhancement of nitric oxide synthase activity in liver cytosol of normal and regucalcin transgenic rats. J Cell Biochem 88(6):1226–1234PubMedCrossRefGoogle Scholar
  151. 151.
    Ma ZJ, Yamaguchi M (2002) Suppressive role of endogenous regucalcin in the regulation of nitric oxide synthase activity in heart muscle cytosol of normal and regucalcin transgenic rats. Int J Mol Med 10(6):761–766PubMedGoogle Scholar
  152. 152.
    Tobisawa M, Yamaguchi M (2003) Role of endogenous regucalcin in brain function: suppression of cytosolic nitric oxide synthase and nuclear protein tyrosine phosphatase activities in brain tissue of transgenic rats. Int J Mol Med 12(4):581–585PubMedGoogle Scholar
  153. 153.
    Nakagawa T, Yamaguchi M (2007) Overexpression of regucalcin suppresses cell response for tumor necrosis factor-alpha or transforming growth factor-beta1 in cloned normal rat kidney proximal tubular epithelial NRK52E cells. J Cell Biochem 100(5):1178–1190PubMedCrossRefGoogle Scholar
  154. 154.
    Sugiura R, Sio SO, Shuntoh H, Kuno T (2002) Calcineurin phosphatase in signal transduction: lessons from fission yeast. Genes Cells 7(7):619–627PubMedCrossRefGoogle Scholar
  155. 155.
    Rusnak F, Mertz P (2000) Calcineurin: form and function. Physiol Rev 80(4):1483–1521PubMedGoogle Scholar
  156. 156.
    Omura M, Yamaguchi M (1998) Inhibition of Ca2 +/calmodulin-dependent phosphatase activity by regucalcin in rat liver cytosol: involvement of calmodulin binding. J Cell Biochem 71(1):140–148PubMedCrossRefGoogle Scholar
  157. 157.
    Omura M, Yamaguchi M (1999) Effect of anti-regucalcin antibody on neutral phosphatase activity in rat liver cytosol: involvement of endogenous regucalcin. Mol Cell Biochem 197(1–2):25–29PubMedCrossRefGoogle Scholar
  158. 158.
    Omura M, Kurota H, Yamaguchi M (1998) Inhibitory effect of regucalcin on Ca2 +/calmodulin-dependent phosphatase activity in rat renal cortex cytosol. Biol Pharm Bull 21(5):440–443PubMedCrossRefGoogle Scholar
  159. 159.
    Morooka Y, Yamaguchi M (2001) Suppressive role of endogenous regucalcin in the regulation of protein phosphatase activity in rat renal cortex cytosol. J Cell Biochem 81(4):639–646PubMedCrossRefGoogle Scholar
  160. 160.
    Morooka Y, Yamaguchi M (2001) Inhibitory effect of regucalcin on protein phosphatase activity in the nuclei of rat kidney cortex. J Cell Biochem 83(1):111–120PubMedCrossRefGoogle Scholar
  161. 161.
    Morooka Y, Yamaguchi M (2002) Endogenous regucalcin suppresses the enhancement of protein phosphatase activity in the cytosol and nucleus of kidney cortex in calcium-administered rats. J Cell Biochem 85(3):553–560PubMedCrossRefGoogle Scholar
  162. 162.
    Ichikawa E, Tsurusaki Y, Yamaguchi M (2004) Suppressive effect of regucalcin on protein phosphatase activity in the heart cytosol of normal and regucalcin transgenic rats. Int J Mol Med 13(2):289–293PubMedGoogle Scholar
  163. 163.
    Hamano T, Yamaguchi M (1999) Inhibitory effect of regucalcin on Ca2 +/calmodulin-dependent protein phosphatase activity in rat brain cytosol. Int J Mol Med 3(6):615–619PubMedGoogle Scholar
  164. 164.
    Yamaguchi M, Hamano T, Misawa H (2000) Expression of Ca(2 +)-binding protein regucalcin in rat brain neurons: inhibitory effect on protein phosphatase activity. Brain Res Bull 52(5):343–348PubMedCrossRefGoogle Scholar
  165. 165.
    Tobisawa M, Yamaguchi M (2003) Suppressive effect of endogenous regucalcin on protein tyrosine phosphatase activity in the nucleus of rat brain: attenuation with increasing age. Int J Mol Med 11(2):205–210PubMedGoogle Scholar
  166. 166.
    Tobisawa M, Tsurusaki Y, Yamaguchi M (2003) Decrease in regucalcin level and enhancement of protein tyrosine phosphatase activity in rat brain microsomes with increasing age. Int J Mol Med 12(4):577–580PubMedGoogle Scholar
  167. 167.
    Yamaguchi M, Katsumata T (1999) Enhancement of protein kinase activity in the cytosol of regenerating rat liver: regulatory role of endogenous regucalcin. Int J Mol Med 3(5):505–510PubMedGoogle Scholar
  168. 168.
    Mori S, Yamaguchi M (1990) Hepatic calcium-binding protein regucalcin decreases Ca2 +/calmodulin-dependent protein kinase activity in rat liver cytosol. Chem Pharm Bull (Tokyo) 38(8):2216–2218CrossRefGoogle Scholar
  169. 169.
    Yamaguchi M, Mori S (1990) Inhibitory effect of calcium-binding protein regucalcin on protein kinase C activity in rat liver cytosol. Biochem Med Metab Biol 43(2):140–146PubMedCrossRefGoogle Scholar
  170. 170.
    Kurota H, Yamaguchi M (1998) Inhibitory effect of calcium-binding protein regucalcin on protein kinase C activity in rat renal cortex cytosol. Biol Pharm Bull 21(4):315–318PubMedCrossRefGoogle Scholar
  171. 171.
    Kurota H, Yamaguchi M (1997) Inhibitory effect of regucalcin on Ca2 +/calmodulin-dependent protein kinase activity in rat renal cortex cytosol. Mol Cell Biochem 177(1–2):239–243PubMedCrossRefGoogle Scholar
  172. 172.
    Hamano T, Yamaguchi M (2001) Inhibitory role of regucalcin in the regulation of Ca2 + dependent protein kinases activity in rat brain neurons. J Neurol Sci 183(1):33–38PubMedCrossRefGoogle Scholar
  173. 173.
    Hamano T, Hanahisa Y, Yamaguchi M (1999) Inhibitory effect of regucalcin on Ca(2 +)-dependent protein kinase activity in rat brain cytosol: involvement of endogenous regucalcin. Brain Res Bull 50(3):187–192PubMedCrossRefGoogle Scholar
  174. 174.
    Wu HY, Tomizawa K, Matsui H (2007) Calpain-calcineurin signaling in the pathogenesis of calcium-dependent disorder. Acta Med Okayama 61(3):123–137PubMedGoogle Scholar
  175. 175.
    Liu X, Van Vleet T, Schnellmann RG (2004) The role of calpain in oncotic cell death. Annu Rev Pharmacol Toxicol 44:349–370PubMedCrossRefGoogle Scholar
  176. 176.
    Baba T, Yamaguchi M (1999) Stimulatory effect of regucalcin on proteolytic activity in rat renal cortex cytosol: involvement of thiol proteases. Mol Cell Biochem 195(1–2):87–92PubMedCrossRefGoogle Scholar
  177. 177.
    Yamaguchi M, Tai H (1992) Calcium-binding protein regucalcin increases calcium-independent proteolytic activity in rat liver cytosol. Mol Cell Biochem 112(1):89–95PubMedCrossRefGoogle Scholar
  178. 178.
    Yamaguchi M, Nishina N (1995) Characterization of regucalcin effect on proteolytic activity in rat liver cytosol: relation to cysteinyl-proteases. Mol Cell Biochem 148(1):67–72PubMedCrossRefGoogle Scholar
  179. 179.
    Linster CL, Van Schaftingen E (2007) Vitamin C. Biosynthesis, recycling and degradation in mammals. FEBS J 274(1):1–22PubMedCrossRefGoogle Scholar
  180. 180.
    Koike K, Kondo Y, Sekiya M, Sato Y, Tobino K, Iwakami SI, Goto S, Takahashi K, Maruyama N, Seyama K, Ishigami A (2010) Complete lack of vitamin C intake generates pulmonary emphysema in senescence marker protein-30 knockout mice. Am J Physiol Lung Cell Mol Physiol 298(6):L784–L792PubMedCrossRefGoogle Scholar
  181. 181.
    Kondo Y, Sasaki T, Sato Y, Amano A, Aizawa S, Iwama M, Handa S, Shimada N, Fukuda M, Akita M, Lee J, Jeong KS, Maruyama N, Ishigami A (2008) Vitamin C depletion increases superoxide generation in brains of SMP30/GNL knockout mice. Biochem Biophys Res Commun 377(1):291–296PubMedCrossRefGoogle Scholar
  182. 182.
    Sato Y, Kajiyama S, Amano A, Kondo Y, Sasaki T, Handa S, Takahashi R, Fukui M, Hasegawa G, Nakamura N, Fujinawa H, Mori T, Ohta M, Obayashi H, Maruyama N, Ishigami A (2008) Hydrogen-rich pure water prevents superoxide formation in brain slices of vitamin C-depleted SMP30/GNL knockout mice. Biochem Biophys Res Commun 375(3):346–350PubMedCrossRefGoogle Scholar
  183. 183.
    Son TG, Zou Y, Jung KJ, Yu BP, Ishigami A, Maruyama N, Lee J (2006) SMP30 deficiency causes increased oxidative stress in brain. Mech Ageing Dev 127(5):451–457PubMedCrossRefGoogle Scholar
  184. 184.
    Sato T, Seyama K, Sato Y, Mori H, Souma S, Akiyoshi T, Kodama Y, Mori T, Goto S, Takahashi K, Fukuchi Y, Maruyama N, Ishigami A (2006) Senescence marker protein-30 protects mice lungs from oxidative stress, aging, and smoking. Am J Respir Crit Care Med 174(5):530–537PubMedCrossRefGoogle Scholar
  185. 185.
    Ambs S, Glynn SA (2011) Candidate pathways linking inducible nitric oxide synthase to a basal-like transcription pattern and tumor progression in human breast cancer. Cell Cycle 10(4):619–624PubMedCrossRefGoogle Scholar
  186. 186.
    Izumi T, Tsurusaki Y, Yamaguchi M (2003) Suppressive effect of endogenous regucalcin on nitric oxide synthase activity in cloned rat hepatoma H4-II-E cells overexpressing regucalcin. J Cell Biochem 89(4):800–807PubMedCrossRefGoogle Scholar
  187. 187.
    Ogita K, Takagi R, Oyama N, Okuda H, Ito F, Okui M, Shimizu N, Yoneda Y (2001) Decrease in level of APG-2, a member of the heat shock protein 110 family, in murine brain following systemic administration of kainic acid. Neuropharmacology 41(3):285–293PubMedCrossRefGoogle Scholar
  188. 188.
    Zheng XY, Zhang HL, Luo Q, Zhu J (2011) Kainic acid-induced neurodegenerative model: potentials and limitations. J Biomed Biotechnol 2011:457079PubMedCentralPubMedCrossRefGoogle Scholar
  189. 189.
    Makker K, Agarwal A, Sharma R (2009) Oxidative stress & male infertility. Indian J Med Res 129(4):357–367PubMedGoogle Scholar
  190. 190.
    Crowell JA, Steele VE, Sigman CC, Fay JR (2003) Is inducible nitric oxide synthase a target for chemoprevention? Mol Cancer Ther 2(8):815–823PubMedGoogle Scholar
  191. 191.
    Lim S, Song BW, Cha MJ, Choi EJ, Ham O, Lee CY, Choi SY, Lee SY, Jang Y, Hwang KC (2009) Differential expression of regucalcin (SMP30) and its function in hypoxic cardiomyocytes. Tissue Eng Regen Med 6(13):1273–1281Google Scholar
  192. 192.
    Izumi T, Yamaguchi M (2004) Overexpression of regucalcin suppresses cell death and apoptosis in cloned rat hepatoma H4-II-E cells induced by lipopolysaccharide, PD 98059, dibucaine, or Bay K 8644. J Cell Biochem 93(3):598–608PubMedCrossRefGoogle Scholar
  193. 193.
    Tsurusaki Y, Yamaguchi M (2002) Suppressive role of endogenous regucalcin in the enhancement of deoxyribonucleic acid synthesis activity in the nucleus of regenerating rat liver. J Cell Biochem 85(3):516–522PubMedCrossRefGoogle Scholar
  194. 194.
    Yamaguchi M, Sakurai T (1991) Inhibitory effect of calcium-binding protein regucalcin on Ca2(+)-activated DNA fragmentation in rat liver nuclei. FEBS Lett 279(2):281–284PubMedCrossRefGoogle Scholar
  195. 195.
    Fukaya Y, Yamaguchi M (2005) Overexpression of regucalcin suppresses cell death and apoptosis in cloned rat hepatoma H4-II-E cells induced by insulin or insulin-like growth factor-I. J Cell Biochem 96(1):145–154PubMedCrossRefGoogle Scholar
  196. 196.
    Nakagawa T, Yamaguchi M (2005) Overexpression of regucalcin suppresses apoptotic cell death in cloned normal rat kidney proximal tubular epithelial NRK52E cells: change in apoptosis-related gene expression. J Cell Biochem 96(6):1274–1285PubMedCrossRefGoogle Scholar
  197. 197.
    Ogasawara J, Watanabe-Fukunaga R, Adachi M, Matsuzawa A, Kasugai T, Kitamura Y, Itoh N, Suda T, Nagata S (1993) Lethal effect of the anti-Fas antibody in mice. Nature 364(6440):806–809PubMedCrossRefGoogle Scholar
  198. 198.
    Elchuri S, Naeemuddin M, Sharpe O, Robinson WH, Huang TT (2007) Identification of biomarkers associated with the development of hepatocellular carcinoma in CuZn superoxide dismutase deficient mice. Proteomics 7(12):2121–2129PubMedCentralPubMedCrossRefGoogle Scholar
  199. 199.
    Kim W, Oe Lim S, Kim JS, Ryu YH, Byeon JY, Kim HJ, Kim YI, Heo JS, Park YM, Jung G (2003) Comparison of proteome between hepatitis B virus- and hepatitis C virus-associated hepatocellular carcinoma. Clin Cancer Res 9(15):5493–5500PubMedGoogle Scholar
  200. 200.
    Jahchan NS, Luo K (2010) SnoN in mammalian development, function and diseases. Curr Opin Pharmacol 10(6):670–675PubMedCentralPubMedCrossRefGoogle Scholar
  201. 201.
    Lamouille S, Derynck R (2009) Oncogene and tumour suppressor: the two faces of SnoN. EMBO J 28(22):3459–3460PubMedCrossRefGoogle Scholar
  202. 202.
    Dallaglio K, Marconi A, Pincelli C (2012) Survivin: a dual player in healthy and diseased skin. J Invest Dermatol 132(1):18–27PubMedCrossRefGoogle Scholar

Copyright information

© Springer Basel 2013

Authors and Affiliations

  • Ricardo Marques
    • 1
  • Cláudio J. Maia
    • 1
  • Cátia Vaz
    • 1
  • Sara Correia
    • 1
  • Sílvia Socorro
    • 1
    Email author
  1. 1.CICS-UBI, Health Sciences Research CentreUniversity of Beira InteriorCovilhãPortugal

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