Stanniocalcin-1 suppresses superoxide generation in macrophages through induction of mitochondrial UCP2

Journal of Leukocyte Biology

Volumn 86, Issue 4, 2009, Pages 981-988

  Wang, Yanlin ^a   Huang, Luping ^a   Abdelrahim, Maen ^b   Cai, Qingsong ^a   Truong, Anh ^a   Bick, Roger ^c   Poindexter, Brian ^c   Sheikh Hamad, David ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b M D ANDERSON CANCER CENTER ORLANDO   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis; Free radicals; Gene regulation; Lipopolysaccharide; Monocytes; Uncoupling proteins

Indexed keywords

ADENOSINE TRIPHOSPHATE; HYPOCALCIN; LIPOPOLYSACCHARIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; STANNIOCALCIN 1; SUPEROXIDE; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL DEATH; CELL FUNCTION; CELL LEVEL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENERGY METABOLISM; IMMUNE RESPONSE; MACROPHAGE; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; CELL LINE; CELL MOVEMENT; ELECTRON TRANSPORT; G1 PHASE; GENE EXPRESSION REGULATION; GLYCOPROTEINS; ION CHANNELS; MACROPHAGES, PERITONEAL; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NADPH OXIDASE; NECROSIS; PROTEIN TRANSPORT; SUPEROXIDES; TIME FACTORS;

MAMMALIA;

EID: 70349637849     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0708454     Document Type: Article

References (60)

1. Fontaine, M. (1964) [Stannius' corpuscles and ionic (CA, K, NA) of the interior environment of the eel (Anguilla Anguilla L.)]. C. R. Hebd. Seances Acad. Sci. 259, 875-878.
2. Stannius, H. (1939) Uber nebenniere bei knochenfischen. Arch. Anat. Physiol. 6, 97-101.
3. Pang, P. K., Pang, R. K., Sawyer, W. H. (1973) Effects of environmental calcium and replacement therapy on the killifish, Fundulus heteroclitus, after the surgical removal of the corpuscles of Stannius. Endocrinology 93, 705-710.
4. Lafeber, F. P., Flik, G., Wendelaar Bonga, S. E., Perry, S. F. (1988) Hypocalcin from Stannius corpuscles inhibits gill calcium uptake in trout. Am. J. Physiol. 254, R891-R896.
5. Moore, E. E., Kuestner, R. E., Conklin, D. C., Whitmore, T. E., Downey, W., Buddle, M. M., Adams, R. L., Bell, L. A., Thompson, D. L., Wolf, A., Chen, L., Stamm, M. R., Grant, F. J., Lok, S., Ren, H., De Jongh, K. S. (1999) Stanniocalcin 2: characterization of the protein and its localization to human pancreatic α cells. Horm. Metab. Res. 31, 406-414. (Pubitemid 29352613)
6. De Niu, P., Radman, D. P., Jaworski, E. M., Deol, H., Gentz, R., Su, J., Olsen, H. S., Wagner, G. F. (2000) Development of a human stanniocalcin radioimmunoassay: serum and tissue hormone levels and pharmacokinetics in the rat. Mol. Cell. Endocrinol. 162, 131-144. (Pubitemid 30347456)
7. Deol, H. K., Varghese, R., Wagner, G. F., DiMattia, G. E. (2000) Dynamic regulation of mouse ovarian stanniocalcin expression during gestation and lactation. Endocrinology 141, 3412-3421. (Pubitemid 32269031)
8. James, K., Seitelbach, M., McCudden, C. R., Wagner, G. F. (2005) Evidence for stanniocalcin binding activity in mammalian blood and glomerular filtrate. Kidney Int. 67, 477-482. (Pubitemid 40139839)
9. Varghese, R., Wong, C. K., Deol, H., Wagner, G. F., DiMattia, G. E. (1998) Comparative analysis of mammalian stanniocalcin genes. Endocrinology 139, 4714-4725. (Pubitemid 28487791)
10. Wong, C. K., Ho, M. A., Wagner, G. F. (1998) The co-localization of stanniocalcin protein, mRNA and kidney cell markers in the rat kidney. J. Endocrinol. 158, 183-189. (Pubitemid 28342061)
11. Stasko, S. E., DiMattia, G. E., Wagner, G. F. (2001) Dynamic changes in stanniocalcin gene expression in the mouse uterus during early implantation. Mol. Cell. Endocrinol. 174, 145-149.
12. Stasko, S. E., Wagner, G. F. (2001) Stanniocalcin gene expression during mouse urogenital development: a possible role in mesenchymal-epithelial signaling. Dev. Dyn. 220, 49-59.
13. Iyer, V. R., Eisen, M. B., Ross, D. T., Schuler, G., Moore, T., Lee, J. C., Trent, J. M., Staudt, L. M., Hudson Jr., J., Boguski, M. S., Lashkari, D., Shalon, D., Botstein, D., Brown, P. O. (1999) The transcriptional program in the response of human fibroblasts to serum 2. Science 283, 83-87. (Pubitemid 29044852)
14. McCudden, C. R., James, K. A., Hasilo, C., Wagner, G. F. (2002) Characterization of mammalian stanniocalcin receptors. Mitochondrial targeting of ligand and receptor for regulation of cellular metabolism. J. Biol. Chem. 277, 45249-45258. (Pubitemid 36159130)
15. Kahn, J., Mehraban, F., Ingle, G., Xin, X., Bryant, J. E., Vehar, G., Schoenfeld, J., Grimaldi, C. J., Peale, F., Draksharapu, A., Lewin, D. A., Gerritsen, M. E. (2000) Gene expression profiling in an in vitro model of angiogenesis. Am. J. Pathol. 156, 1887-1900. (Pubitemid 30641758)
16. Paciga, M., McCudden, C. R., Londos, C., DiMattia, G. E., Wagner, G. F. (2003) Targeting of big stanniocalcin and its receptor to lipid storage droplets of ovarian steroidogenic cells. J. Biol. Chem. 278, 49549-49554.
17. Yoshiko, Y., Aubin, J. E., Maeda, N. (2002) Stanniocalcin 1 (STC1) protein and mRNA are developmentally regulated during embryonic mouse osteogenesis: the potential of STC1 as an autocrine/paracrine factor for osteoblast development and bone formation. J. Histochem. Cytochem. 50, 483-492. (Pubitemid 34250587)
18. Filvaroff, E. H., Guillet, S., Zlot, C., Bao, M., Ingle, G., Steinmetz, H., Hoeffel, J., Bunting, S., Ross, J., Carano, R. A., Powell-Braxton, L., Wagner, G. F., Eckert, R., Gerritsen, M. E., French, D. M. (2002) Stanniocalcin 1 alters muscle and bone structure and function in transgenic mice. Endocrinology 143, 3681-3690. (Pubitemid 34925745)
19. Madsen, K. L., Tavernini, M. M., Yachimec, C., Mendrick, D. L., Alfonso, P. J., Buergin, M., Olsen, H. S., Antonaccio, M. J., Thomson, A. B., Fedorak, R. N. (1998) Stanniocalcin: a novel protein regulating calcium and phosphate transport across mammalian intestine. Am. J. Physiol. 274, G96-102. (Pubitemid 128736024)
20. Wagner, G. F., Vozzolo, B. L., Jaworski, E., Haddad, M., Kline, R. L., Olsen, H. S., Rosen, C. A., Davidson, M. B., Renfro, J. L. (1997) Human stanniocalcin inhibits renal phosphate excretion in the rat. J. Bone Miner. Res. 12, 165-171. (Pubitemid 27086296)
21. Chang, A. C., Jellinek, D. A., Reddel, R. R. (2003) Mammalian stanniocalcins and cancer. Endocr. Relat. Cancer 10, 359-373.
22. Kanellis, J., Bick, R., Garcia, G., Truong, L., Tsao, C. C., Etemadmoghadam, D., Poindexter, B., Feng, L., Johnson, R. J., Sheikh-Hamad, D. (2004) Stanniocalcin-1, an inhibitor of macrophage chemotaxis and chemokinesis. Am. J. Physiol. Renal Physiol. 286, F356-F362. (Pubitemid 38141680)
23. Chakraborty, A., Brooks, H., Zhang, P., Smith, W., McReynolds, M. R., Hoying, J. B., Bick, R., Truong, L., Poindexter, B., Lan, H., Elbjeirami, W., Sheikh-Hamad, D. (2007) Stanniocalcin-1 regulates endothelial gene expression and modulates transendothelial migration of leukocytes. Am. J. Physiol. Renal Physiol. 292, F895-F904. (Pubitemid 46220559)
24. Chen, C., Jamaluddin, M. S., Yan, S., Sheikh-Hamad, D., Yao, Q. (2008) Human stanniocalcin-1 blocks TNF-α-induced monolayer permeability in human coronary artery endothelial cells. Arterioscler. Thromb. Vasc. Biol. 28, 906-912. (Pubitemid 351544106)
25. Ellard, J. P., McCudden, C. R., Tanega, C., James, K. A., Ratkovic, S., Staples, J. F., Wagner, G. F. (2007) The respiratory effects of stanniocalcin-1 (STC-1) on intact mitochondria and cells: STC-1 uncouples oxidative phosphorylation and its actions are modulated by nucleotide triphosphates. Mol. Cell. Endocrinol. 264, 90-101. (Pubitemid 46097304)
26. Saito, A., Sakurai, H., Saito, T., Taji, S., Miyagami, T., Suzuki, N., Seitz, H. M., Osaki, H. (1987) Correlation between release of reactive oxygen intermediates and inhibition of Toxoplasma multiplication in mouse peritoneal and alveolar macrophages and kidney cells after in vitro incubation with Obioactin, lonomycin A, muramyl dipeptide, lipopolysaccharide or Toxoplasma lysate antigen. Zentralbl. Bakteriol. Mikrobiol. Hyg. [A] 264, 446-454.
27. Zhang, J., Alfonso, P., Thotakura, N. R., Su, J., Buergin, M., Parmelee, D., Collins, A. W., Oelkuct, M., Gaffney, S., Gentz, S., Radman, D. P., Wagner, G. F., Gentz, R. (1998) Expression, purification, and bioassay of human stanniocalcin from baculovirus-infected insect cells and recombinant CHO cells. Protein Expr. Purif. 12, 390-398. (Pubitemid 28360434)
28. Wendelaar Bonga, S. E., Smits, P. W., Flik, G., Kaneko, T., Pang, P. K. (1989) Immunocytochemical localization of hypocalcin in the endocrine cells of the corpuscles of Stannius in three teleost species (trout, flounder and goldfish). Cell Tissue Res. 255, 651-656.
29. Adami, C., Brunda, M. J., Palleroni, A. V. (1993) In vivo immortalization of murine peritoneal macrophages: a new rapid and efficient method for obtaining macrophage cell lines. J. Leukoc. Biol. 53, 475-478. (Pubitemid 23159891)
30. Sottocasa, G. L., Kuylenstierna, B., Ernster, L., Bergstrand, A. (1967) An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J. Cell Biol. 32, 415-438.
31. Sherratt, H. S., Watmough, N. J., Johnson, M. A., Turnbull, D. M. (1988) Methods for study of normal and abnormal skeletal muscle mitochondria. Methods Biochem. Anal. 33, 243-335.
32. Wang, Y., De Keulenaer, G. W., Lee, R. T. (2002) Vitamin D(3)-up-regulated protein-1 is a stress-responsive gene that regulates cardiomyocyte viability through interaction with thioredoxin. J. Biol. Chem. 277, 26496-26500. (Pubitemid 34967145)
33. Darzynkiewicz, Z., Huang, X., Okafuji, M., King, M. A. (2004) Cytometric methods to detect apoptosis. Methods Cell Biol. 75, 307-341.
34. Darzynkiewicz, Z., Juan, G., Bedner, E. (2001) Determining cell cycle stages by flow cytometry. Curr. Protoc. Cell Biol. May, 8.4.
35. Darzynkiewicz, Z., Huang, X. (2004) Analysis of cellular DNA content by flow cytometry. Curr. Protoc. Immunol. May, 5.7.
36. Choi, H. S., Kim, J. W., Cha, Y. N., Kim, C. (2006) A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells. J. Immunoassay Immunochem. 27, 31-44.
37. Rousset, S., Alves-Guerra, M. C., Mozo, J., Miroux, B., Cassard-Doulcier, A. M., Bouillaud, F., Ricquier, D. (2004) The biology of mitochondrial uncoupling proteins. Diabetes 53, S130-S135.
38. Nishio, K., Qiao, S., Yamashita, H. (2005) Characterization of the differential expression of uncoupling protein 2 and ROS production in differentiated mouse macrophage-cells (Mm1) and the progenitor cells (M1). J. Mol. Histol. 36, 35-44. (Pubitemid 40614380)
39. Bai, Y., Onuma, H., Bai, X., Medvedev, A. V., Misukonis, M., Weinberg, J. B., Cao, W., Robidoux, J., Floering, L. M., Daniel, K. W., Collins, S. (2005) Persistent nuclear factor-κ B activation in Ucp2-/- mice leads to enhanced nitric oxide and inflammatory cytokine production. J. Biol. Chem. 280, 19062-19069. (Pubitemid 41379612)
40. Arsenijevic, D., Onuma, H., Pecqueur, C., Raimbault, S., Manning, B. S., Miroux, B., Couplan, E., Alves-Guerra, M. C., Goubern, M., Surwit, R., Bouillaud, F., Richard, D., Collins, S., Ricquier, D. (2000) Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat. Genet. 26, 435-439.
41. Emre, Y., Hurtaud, C., Nubel, T., Criscuolo, F., Ricquier, D., Cassard- Doulcier, A. M. (2007) Mitochondria contribute to LPS-induced MAPK activation via uncoupling protein UCP2 in macrophages. Biochem. J. 402, 271-278.
42. Ishioka, K., Kanehira, K., Sasaki, N., Kitamura, H., Kimura, K., Saito, M. (2002) Canine mitochondrial uncoupling proteins: structure and mRNA expression of three isoforms in adult beagles. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 131, 483-489. (Pubitemid 34214869)
43. Sack, M. N. (2006) Mitochondrial depolarization and the role of uncoupling proteins in ischemia tolerance. Cardiovasc. Res. 72, 210-219. (Pubitemid 44515171)
44. Korshunov, S. S., Skulachev, V. P., Starkov, A. A. (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 416, 15-18.
45. Saikumar, P., Dong, Z., Patel, Y., Hall, K., Hopfer, U., Weinberg, J. M., Venkatachalam, M. A. (1998) Role of hypoxia-induced Bax translocation and cytochrome c release in reoxygenation injury. Oncogene 17, 3401-3415. (Pubitemid 29050675)
46. Kubota, Y., Takahashi, S., Sato, H., Suetomi, K. (2005) Radiation-induced apoptosis in peritoneal resident macrophages of C3H mice: selective involvement of superoxide anion, but not other reactive oxygen species. Int. J. Radiat. Biol. 81, 459-472. (Pubitemid 41657562)
47. Madesh, M., Hawkins, B. J., Milovanova, T., Bhanumathy, C. D., Joseph, S. K., Ramachandrarao, S. P., Sharma, K., Kurosaki, T., Fisher, A. B. (2005) Selective role for superoxide in InsP3 receptor-mediated mitochondrial dysfunction and endothelial apoptosis. J. Cell Biol. 170, 1079-1090. (Pubitemid 41362640)
48. Schultz, B. E., Chan, S. I. (2001) Structures and proton-pumping strategies of mitochondrial respiratory enzymes. Annu. Rev. Biophys. Biomol. Struct. 30, 23-65. (Pubitemid 32566155)
49. Brand, M. D., Esteves, T. C. (2005) Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab. 2, 85-93.
50. Rial, E., Gonzalez-Barroso, M. M. (2001) Physiological regulation of the transport activity in the uncoupling proteins UCP1 and UCP2. Biochim. Biophys. Acta 1504, 70-81.
51. Kim-Han, J. S., Dugan, L. L. (2005) Mitochondrial uncoupling proteins in the central nervous system. Antioxid. Redox Signal. 7, 1173-1181. (Pubitemid 41232512)
52. Tergaonkar, V. (2006) NFκB pathway: a good signaling paradigm and therapeutic target. Int. J. Biochem. Cell Biol. 38, 1647-1653.
53. Serlachius, M., Zhang, K. Z., Andersson, L. C. (2004) Stanniocalcin in terminally differentiated mammalian cells. Peptides 25, 1657-1662. (Pubitemid 39346207)
54. Varghese, R., Gagliardi, A. D., Bialek, P. E., Yee, S. P., Wagner, G. F., DiMattia, G. E. (2002) Overexpression of human stanniocalcin affects growth and reproduction in transgenic mice. Endocrinology 143, 868-876. (Pubitemid 34164035)
55. Clapham, J. C., Arch, J. R., Chapman, H., Haynes, A., Lister, C., Moore, G. B., Piercy, V., Carter, S. A., Lehner, I., Smith, S. A., Beeley, L. J., Godden, R. J., Herrity, N., Skehel, M., Changani, K. K., Hockings, P. D., Reid, D. G., Squires, S. M., Hatcher, J., Trail, B., Latcham, J., Rastan, S., Harper, A. J., Cadenas, S., Buckingham, J. A., Brand, M. D., Abuin, A. (2000) Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 406, 415-418. (Pubitemid 30625561)
56. Mandal, S., Guptan, P., Owusu-Ansah, E., Banerjee, U. (2005) Mitochondrial regulation of cell cycle progression during development as revealed by the tenured mutation in Drosophila. Dev. Cell 9, 843-854. (Pubitemid 41724111)
57. Hattori, T., Nagamatsu, T., Ito, M., Suzuki, Y. (1994) Contribution of ED-1- and CD-8-positive cells to the development of crescentic-type anti- GBM nephritis in rats. Nippon Jinzo Gakkai Shi 36, 1228-1239.
58. Hopfer, H., Maron, R., Butzmann, U., Helmchen, U., Weiner, H. L., Kalluri, R. (2003) The importance of cell-mediated immunity in the course and severity of autoimmune anti-glomerular basement membrane disease in mice. FASEB J. 17, 860-868. (Pubitemid 36538661)
59. Tipping, P. G., Neale, T. J., Holdsworth, S. R. (1985) T lymphocyte participation in antibody-induced experimental glomerulonephritis. Kidney Int. 27, 530-537. (Pubitemid 15076760)
60. Huang, L., Garcia, G., Lou, Y., Zhou, Q., Truong, L. D., Dimattia, G., Lan, X. R., Lan, H. Y., Wang, Y., Sheikh-Hamad, D. (2009) Anti-inflammatory and renal protective actions of stanniocalcin-1 in a model of antiglomerular basement membrane glomerulonephritis. Am. J. Pathol. 174, 1368-1378.