Senescence marker protein 30: Functional and structural insights to its unknown physiological function

Biomolecular Concepts

Volumn 2, Issue 6, 2011, Pages 469-480

  Scott, Stephanie H ^a   Bahnsonand, Brian J ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

b propeller; divalent metal binding; gluconolactonase; oxidative stress; regucalcin; SMP30

Indexed keywords

MAMMALIA; PRIMATES; VERTEBRATA;

EID: 84902821214     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/BMC.2011.041     Document Type: Review

References (81)

1. Fujita T, Uchida K, Maruyama N. Purification of senescence marker protein-30 (SMP30) and its androgen-independent decrease with age in the rat liver. Biochim Biophys Acta 1992; 1116: 122-8.
2. Fujita T, Shirasawa T, Uchida K, Maruyama N. Isolation of cDNA clone encoding rat senescence marker protein-30 (SMP30) and its tissue distribution. Biochim Biophys Acta 1992; 1132: 297-305.
3. Fujita T, Mandel JL, Shirasawa T, Hino O, Shirai T, Maruyama N. Isolation of cDNA clone encoding human homologue of senescence marker protein-30 (SMP30) and its location on the X chromosome. Biochim Biophys Acta 1995; 1263: 249-52.
4. Fujita T, Shirasawa T, Maruyama N. Isolation and characterization of genomic and cDNA clones encoding mouse senescence marker protein-30 (SMP30). Biochim Biophys Acta 1996; 1308: 49-57.
5. Maruyama N, Ishigami A, Kuramoto M, Handa S, Kubo S, Imasawa T, Seyama K, Shimosawa T, Kasahara Y. Senescence marker protein-30 knockout mouse as an aging model. Ann NY Acad Sci 2004; 1019: 383-7.
6. Laurentino SS, Correia S, Cavaco JE, Oliveira PF, Rato L, Sousa M, Barros A, Socorro S. Regucalcin is broadly expressed in male reproductive tissues and a new androgen target gene in mammalian testis. Reproduction 2011; 142: 447-56.
7. Maia CJ, Santos CR, Schmitt F, Socorro S. Regucalcin is expressed in rat mammary gland and prostate and down-regulated by 17b-estradiol. Mol Cell Biochem 2008; 311: 81-6.
8. Yamaguchi M, Yamamoto T. Purification of calcium binding substance from soluble fraction of normal rat liver. Chem Pharm Bull (Tokyo) 1978; 26: 1915-8.
9. Billecke SS, Primo-Parmo SL, Dunlop CS, Doorn JA, La Du BN, Broomfield CA. Characterization of a soluble mouse liver enzyme capable of hydrolyzing diisopropyl phosphorofluoridate. Chem Biol Interact 1999; 119-120: 251-6.
10. Bublitz C, Lehninger AL. The role of aldonolactonase in the conversion of L-gulonate to L-ascorbate. Biochim Biophys Acta 1961; 47: 288-97.
11. Shimokawa N, Yamaguchi M. Molecular cloning and sequencing of the cDNA coding for a calcium-binding protein regucalcin from rat liver. FEBS Lett 1993; 327: 251-5.
12. Kondo Y, Ishigami A, Kubo S, Handa S, Gomi K, Hirokawa K, Kajiyama N, Chiba T, Shimokado K, Maruyama N. Senescence marker protein-30 is a unique enzyme that hydrolyzes diisopropyl phosphorofluoridate in the liver. FEBS Lett 2004; 570: 57-62.
13. Chakraborti S, Bahnson BJ. Crystal structure of human senescence marker protein 30: insights linking structural, enzymatic, and physiological functions. Biochemistry 2010; 49: 3436-44.
14. Fujita T, Inoue H, Kitamura T, Sato N, Shimosawa T, Maruyama N. Senescence marker protein-30 (SMP30) rescues cell death by enhancing plasma membrane Ca2q-pumping activity in Hep G2 cells. Biochem Biophys Res Commun 1998; 250: 374-80.
15. Ishigami A, Fujita T, Handa S, Shirasawa T, Koseki H, Kitamura T, Enomoto N, Sato N, Shimosawa T, Maruyama N. Senescence marker protein-30 knockout mouse liver is highly susceptible to tumor necrosis factor-a- and Fas-mediated apoptosis. Am J Pathol 2002; 161: 1273-81.
16. Yamaguchi M. Role of regucalcin in maintaining cell homeostasis and function. Int J Mol Med 2005; 15: 371-89.
17. Yamaguchi M. Role of regucalcin in calcium signaling. Life Sci 2000; 66: 1769-80.
18. Lehninger AL, Ul Hassan M. Enzymatic formation of ascorbic acid in rat liver extracts. J Biol Chem 1956; 223: 123-38.
19. Winkelman J, Lehninger AL. Aldono- and uronolactonases of animal tissues. J Biol Chem 1958; 233: 794-9.
20. Linster CL, Van Schaftingen E. Vitamin C. Biosynthesis, recycling and degradation in mammals. FEBS J 2007; 274: 1-22.
21. Kondo Y, Inai Y, Sato Y, Handa S, Kubo S, Shimokado K, Goto S, Nishikimi M, Maruyama N, Ishigami A. 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 2006; 103: 5723-8.
22. Yamaguchi M. Regucalcin and metabolic disorders: osteoporosis and hyperlipidemia are induced in regucalcin transgenic rats. Mol Cell Biochem 2010; 341: 119-33.
23. Yamaguchi M, Misawa H, Uchiyama S, Morooka Y, Tsurusaki Y. Role of endogenous regucalcin in bone metabolism: bone loss is induced in regucalcin transgenic rats. Int J Mol Med 2002; 10: 377-83.
24. Hasegawa G. Decreased senescence marker protein-30 could be a factor that contributes to the worsening of glucose tolerance in normal aging. Islets 2010; 2: 258-60.
25. Hasegawa G, Yamasaki M, Kadono M, Tanaka M, Asano M, Senmaru T, Kondo Y, Fukui M, Obayashi H, Maruyama N, Nakamura N, Ishigami A. Senescence marker protein-30/ gluconolactonase deletion worsens glucose tolerance through impairment of acute insulin secretion. Endocrinology 2010; 151: 529-36.
26. Ishigami A, Kondo Y, Nanba R, Ohsawa T, Handa S, Kubo S, Akita M, Maruyama N. SMP30 deficiency in mice causes an accumulation of neutral lipids and phospholipids in the liver and shortens the life span. Biochem Biophys Res Commun 2004; 315: 575-80.
27. 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. Hepatic senescence marker protein- 30 is involved in the progression of nonalcoholic fatty liver disease. J Gastroenterol 2010; 45: 426-34.
28. Yamaguchi M, Igarashi A, Uchiyama S, Sawada N. Hyperlipidemia is induced in regucalcin transgenic rats with increasing age. Int J Mol Med 2004; 14: 647-51.
29. Ishigami T, Fujita T, Simbula G, Columbano A, Kikuchi K, Ishigami A, Shimosawa T, Arakawa Y, Maruyama N. Regulatory effects of senescence marker protein 30 on the proliferation of hepatocytes. Pathol Int 2001; 51: 491-7.
30. Maia C, Santos C, Schmitt F, Socorro S. Regucalcin is underexpressed in human breast and prostate cancers: effect of sex steroid hormones. J Cell Biochem 2009; 107: 667-76.
31. Ishigami A, Handa S, Maruyama N, Supakar PC. Nuclear localization of senescence marker protein-30, SMP30, in cultured mouse hepatocytes and its similarity to RNA polymerase. Biosci Biotechnol Biochem 2003; 67: 158-60.
32. Misawa H, Yamaguchi M. The gene of Ca2q-binding protein regucalcin is highly conserved in vertebrate species. Int J Mol Med 2000; 6: 191-6.
33. Shimokawa N, Isogai M, Yamaguchi M. Specific species and tissue differences for the gene expression of calcium-binding protein regucalcin. Mol Cell Biochem 1995; 143: 67-71.
34. Gomi K, Hirokawa K, Kajiyama N. Molecular cloning and expression of the cDNAs encoding luciferin-regenerating enzyme from Luciola cruciata and Luciola lateralis. Gene 2002; 294: 157-66.
35. Day JC, Bailey MJ. Structure and evolution of the luciferinregenerating enzyme (LRE) gene from the firefly Photinus pyralis. Insect Mol Biol 2003; 12: 365-72.
36. Gomi K, Kajiyama N. Oxyluciferin, a luminescence product of firefly luciferase, is enzymatically regenerated into luciferin. J Biol Chem 2001; 276: 36508-13.
37. Goto SG. Expression of Drosophila homologue of senescence marker protein-30 during cold acclimation. J Insect Physiol 2000; 46: 1111-20.
38. Nakajima Y, Natori S. Identification and characterization of an anterior fat body protein in an insect. J Biochem 2000; 127: 901-8.
39. Gupta SD, Chaudhuri CR, Chatterjee IB. Incapability of L-ascorbic acid synthesis by insects. Arch Biochem Biophys 1972; 152: 889-90.
40. Kramer KJ, Seib PA. Ascorbic acid and the growth and development of insects. Adv Chem Ser 1982; 200: 275-91.
41. Prosser CL, editor. Environmental and metabolic animal physiology. 4th ed., New York: Wiley-Liss, 1991.
42. Stone I. Natural history of ascorbic acid in evolution of mammals and primates and its significance for present-day man. Orthomol Psych 1972; 1: 82-9.
43. Chaudhuri CR, Chatterjee IB. L-Ascorbic acid synthesis in birds: phylogenetic trend. Science 1969; 164: 435-6.
44. Elliot O, Yess NJ, Hegsted DM. Biosynthesis of ascorbic acid in tree shrew and slow loris. Nature 1966; 212: 739-40.
45. Inoue HFT, Kitamura T, Shimosawa T, Nagasawa R, Inoue R, Maruyama N, Nagasawa T. Senescence marker protein-30 (SMP30) enhances the calcium efflux from renal tubular epithelial cells. Clin Exp Nephrol 1999; 3: 261-7.
46. Matsuyama S, Kitamura T, Enomoto N, Fujita T, Ishigami A, Handa S, Maruyama N, Zheng D, Ikejima K, Takei Y, Sato N. Senescence marker protein-30 regulates Akt activity and contributes to cell survival in Hep G2 cells. Biochem Biophys Res Commun 2004; 321: 386-90.
47. Takahashi H, Yamaguchi M. Stimulatory effect of regucalcin on ATP-dependent calcium transport in rat liver plasma membranes. Mol Cell Biochem 1997; 168: 149-53.
48. Takahashi H, Yamaguchi M. Role of regucalcin as an activator of Ca2q-ATPase activity in rat liver microsomes. J Cell Biochem 1999; 74: 663-9.
49. Izumi T, Yamaguchi M. Overexpression of regucalcin suppresses cell death in cloned rat hepatoma H4-II-E cells induced by tumor necrosis factor-a or thapsigargin. J Cell Biochem 2004; 92: 296-306.
50. Alikhani M, Alikhani Z, He H, Liu R, Popek BI, Graves DT. Lipopolysaccharides indirectly stimulate apoptosis and global induction of apoptotic genes in fibroblasts. J Biol Chem 2003; 278: 52901-8.
51. Izumi T, Yamaguchi M. 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 2004; 93: 598608.
52. Nakagawa T, Yamaguchi M. Overexpression of regucalcin suppresses apoptotic cell death in cloned normal rat kidney proximal tubular epithelial NRK52E cells: change in apoptosisrelated gene expression. J Cell Biochem 2005; 96: 1274-85.
53. 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. Senescence marker protein-30 protects mice lungs from oxidative stress, aging, and smoking. Am J Respir Crit Care Med 2006; 174: 530-7.
54. Son TG, Zou Y, Jung KJ, Yu BP, Ishigami A, Maruyama N, Lee J. SMP30 deficiency causes increased oxidative stress in brain. Mech Ageing Dev 2006; 127: 451-7.
55. Son TG, Kim SJ, Kim K, Kim MS, Chung HY, Lee J. Cytoprotective roles of senescence marker protein 30 against intracellular calcium elevation and oxidative stress. Arch Pharm Res 2008; 31: 872-7.
56. Amano A, Aigaki T, Maruyama N, Ishigami A. Ascorbic acid depletion enhances expression of the sodium-dependent vitamin C transporters, SVCT1 and SVCT2, and uptake of ascorbic acid in livers of SMP30/GNL knockout mice. Arch Biochem Biophys 2010; 496: 38-44.
57. Arai KY, Sato Y, Kondo Y, Kudo C, Tsuchiya H, Nomura Y, Ishigami A, Nishiyama T. Effects of vitamin C deficiency on the skin of the senescence marker protein-30 (SMP30) knockout mouse. Biochem Biophys Res Commun 2009; 385: 478-83.
58. Furusawa H, Sato Y, Tanaka Y, Inai Y, Amano A, Iwama M, Kondo Y, Handa S, Murata A, Nishikimi M, Goto S, Maruyama N, Takahashi R, Ishigami A. Vitamin C is not essential for carnitine biosynthesis in vivo: verification in vitamin C-depleted senescence marker protein-30/gluconolactonase knockout mice. Biol Pharm Bull 2008; 31: 1673-9.
59. Koike K, Kondo Y, Sekiya M, Sato Y, Tobino K, Iwakami S, Goto S, Takahashi K, Maruyama N, Seyama K, Ishigami A. Complete lack of vitamin C intake generates pulmonary emphysema in senescence marker protein-30 knockout mice. Am J Physiol Lung C 2010; 298: L784-L92.
60. 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. Vitamin C depletion increases superoxide generation in brains of SMP30/GNL knockout mice. Biochem Biophys Res Commun 2008; 377: 291-6.
61. 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. Hydrogen-rich pure water prevents superoxide formation in brain slices of vitamin C-depleted SMP30/GNL knockout mice. Biochem Biophys Res Commun 2008; 375: 346-50.
62. Handa S, Maruyama N, Ishigami A. Over-expression of senescence marker protein-30 decreases reactive oxygen species in human hepatic carcinoma Hep G2 cells. Biol Pharm Bull 2009; 32: 1645-8.
63. Costa LG. Current issues in organophosphate toxicology. Clin Chim Acta 2006; 366: 1-13.
64. Draganov DI. Lactonases with organophosphatase activity: structural and evolutionary perspectives. Chem Biol Interact 2010; 187: 370-2.
65. Blum MM, Chen JC. Structural characterization of the catalytic calcium-binding site in diisopropyl fluorophosphatase (DFPase)-comparison with related b-propeller enzymes. Chem Biol Interact 2010; 187: 373-9.
66. Morton DJ, Barrett-Connor EL, Schneider DL. Vitamin C supplement use and bone mineral density in postmenopausal women. J Bone Miner Res 2001; 16: 135-40.
67. Gabbay KH, Bohren KM, Morello R, Bertin T, Liu J, Vogel P. Ascorbate synthesis pathway: dual role of ascorbate in bone homeostasis. J Biol Chem 2010; 285: 19510-20.
68. Uchiyama S, Yamaguchi M. Bone loss in regucalcin transgenic rats: enhancement of osteoclastic cell formation from bone marrow of rats with increasing age. Int J Mol Med 2004; 14: 451-5.
69. Yamaguchi M, Sawada N, Uchiyama S, Misawa H, Ma ZJ. Expression of regucalcin in rat bone marrow cells: involvement of osteoclastic bone resorption in regucalcin transgenic rats. Int J Mol Med 2004; 13: 437-43.
70. Bayard M, Holt J, Boroughs E. Nonalcoholic fatty liver disease. Am Fam Physician 2006; 73: 1961-8.
71. Chuang JH, Wang PW, Tai MH. An adipocentric view of liver fibrosis and cirrhosis. Chang Gung Med J 2004; 27: 855-68.
72. Cusi K. Nonalcoholic fatty liver disease in type 2 diabetes mellitus. Curr Opin Endocrinol Diabetes Obes 2009; 16: 141-9.
73. Lv S, Wang JH, Liu F, Gao Y, Fei R, Du SC, Wei L. Senescence marker protein 30 in acute liver failure: validation of a mass spectrometry proteomics assay. BMC Gastroenterol 2008; 8: 17.
74. Park JK, Ki MR, Lee HR, Hong IH, Ji AR, Ishigami A, Park SI, Kim JM, Chung HY, Yoo SE, Jeong KS. Vitamin C deficiency attenuates liver fibrosis by way of up-regulated peroxisome proliferator-activated receptor-g expression in senescence marker protein 30 knockout mice. Hepatology 2010; 51: 1766-77.
75. Nakashima C, Yamaguchi M. Overexpression of regucalcin suppresses gene expression of insulin signaling-related proteins in cloned rat hepatoma H4-II-E cells: involvement of insulin resistance. Int J Mol Med 2007; 20: 709-16.
76. Murata T, Shinya N, Yamaguchi M. Expression of calciumbinding protein regucalcin mRNA in the cloned human hepatoma cells (HepG2): stimulation by insulin. Mol Cell Biochem 1997; 175: 163-8.
77. Nakagawa T, Sawada N, Yamaguchi M. Overexpression of regucalcin suppresses cell proliferation of cloned normal rat kidney proximal tubular epithelial NRK52E cells. Int J Mol Med 2005; 16: 637-43.
78. Yamaguchi M, Daimon Y. Overexpression of regucalcin suppresses cell proliferation in cloned rat hepatoma H4-II-E cells: involvement of intracellular signaling factors and cell cyclerelated genes. J Cell Biochem 2005; 95: 1169-77.
79. Tsurusaki Y, Yamaguchi M. Overexpression of regucalcin modulates tumor-related gene expression in cloned rat hepatoma H4-II-E cells. J Cell Biochem 2003; 90: 619-26.
80. Tsurusaki Y, Yamaguchi M. Role of regucalcin in liver nuclear function: binding of regucalcin to nuclear protein or DNA and modulation of tumor-related gene expression. Int J Mol Med 2004; 14: 277-81.
81. Subramaniam S. The Biology Workbench-a seamless database and analysis environment for the biologist. Proteins 1998; 32: 1-2.