109
Views
138
CrossRef citations to date
0
Altmetric
Cell Growth and Development

Characterization of Stanniocalcin 2, a Novel Target of the Mammalian Unfolded Protein Response with Cytoprotective Properties

, , , , , , , & show all
Pages 9456-9469 | Received 17 Mar 2004, Accepted 10 Aug 2004, Published online: 27 Mar 2023

REFERENCES

  • Berridge, M. J. 2002. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32:235–249.
  • Brummelkamp, T. R., Bernards R., and Agami R.. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550–553.
  • Butkus, A., Roche P. J., Fernley R. T., Haralambidis J., Penschow J. D., Ryan G. B., Trahair J. F., Tregear G. W., and Coghlan J. P.. 1987. Purification and cloning of a corpuscles of Stannius protein from Anguilla australis. Mol. Cell Endocrinol. 54:123–133.
  • Calfon, M., Zeng H., Urano F., Till J. H., Hubbard S. R., Harding H. P., Clark S. G., and Ron D.. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92–96.
  • Casagrande, R., Stern P., Diehn M., Shamu C., Osario M., Zuniga M., Brown P. O., and Ploegh H.. 2000. Degradation of proteins from the ER of Saccharomyces cerevisiae requires an intact unfolded protein response pathway. Mol. Cell 5:729–735.
  • Caspersen, C., Pedersen P. S., and Treiman M.. 2000. The sarco/endoplasmic reticulum calcium-ATPase 2b is an endoplasmic reticulum stress-inducible protein. J. Biol. Chem. 275:22363–22372.
  • Chang, A. C., Jellinek D. A., and Reddel R. R.. 2003. Mammalian stanniocalcins and cancer. Endocrinol. Relat. Cancer 10:359–373.
  • Chang, A. C., and Reddel R. R.. 1998. Identification of a second stanniocalcin cDNA in mouse and human: stanniocalcin 2. Mol. Cell Endocrinol. 141:95–99.
  • DiMattia, G. E., Varghese R., and Wagner G. F.. 1998. Molecular cloning and characterization of stanniocalcin-related protein. Mol. Cell Endocrinol. 146:137–140.
  • Ermak, G., and Davies K. J.. 2002. Calcium and oxidative stress: from cell signaling to cell death. Mol. Immunol. 38:713–721.
  • Forman, M. S., Lee V. M., and Trojanowski J. Q.. 2003. ′Unfolding' pathways in neurodegenerative disease. Trends Neurosci. 26:407–410.
  • Harding, H. P., Calfon M., Urano F., Novoa I., and Ron D.. 2002. Transcriptional and translational control in the mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18:575–599.
  • Harding, H. P., and Ron D.. 2002. Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51(Suppl. 3):S455–S461.
  • Harding, H. P., Zeng H., Zhang Y., Jungries R., Chung P., Plesken H., Sabatini D. D., and Ron D.. 2001. Diabetes mellitus and exocrine pancreatic dysfunction in perk−/− mice reveals a role for translational control in secretory cell survival. Mol. Cell 7:1153–1163.
  • Harding, H. P., Zhang Y., Bertolotti A., Zeng H., and Ron D.. 2000. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5:897–904.
  • Harding, H. P., Zhang Y., and Ron D.. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271–274.
  • Harding, H. P., Zhang Y., Zeng H., Novoa I., Lu P. D., Calfon M., Sadri N., Yun C., Popko B., Paules R., Stojdl D. F., Bell J. C., Hettmann T., Leiden J. M., and Ron D.. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11:619–633.
  • Hasan, M. T., Chang C. C., and Chang T. Y.. 1994. Somatic cell genetic and biochemical characterization of cell lines resulting from human genomic DNA transfections of Chinese hamster ovary cell mutants defective in sterol-dependent activation of sterol synthesis and LDL receptor expression. Somat. Cell Mol. Genet. 20:183–194.
  • Haze, K., Yoshida H., Yanagi H., Yura T., and Mori K.. 1999. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10:3787–3799.
  • Holtz, W. A., and O'Malley K. L.. 2003. Parkinsonian mimetics induce aspects of unfolded protein response in death of dopaminergic neurons. J. Biol. Chem. 278:19367–19377.
  • Ishibashi, K., and Imai M.. 2002. Prospect of a stanniocalcin endocrine/paracrine system in mammals. Am. J. Physiol. Renal Physiol. 282:F367–F375.
  • Ishibashi, K., Miyamoto K., Taketani Y., Morita K., Takeda E., Sasaki S., and Imai M.. 1998. Molecular cloning of a second human stanniocalcin homologue (STC2). Biochem. Biophys. Res. Commun. 250:252–258.
  • Ito, D., Imai Y., Ohsawa K., Nakajima K., Fukuuchi Y., and Kohsaka S.. 1998. Microglia-specific localization of a novel calcium binding protein, Iba1. Brain Res. Mol. Brain Res. 57:1–9.
  • Ito, D., Tanaka K., Suzuki S., Dembo T., and Fukuuchi Y.. 2001. Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 32:1208–1215.
  • Ito, D., Tanaka K., Suzuki S., Dembo T., Kosakai A., and Fukuuchi Y.. 2001. Upregulation of the Ire1-mediated signaling molecule, Bip, in ischemic rat brain. Neuroreport 12:4023–4028.
  • Jellinek, D. A., Chang A. C., Larsen M. R., Wang X., Robinson P. J., and Reddel R. R.. 2000. Stanniocalcin 1 and 2 are secreted as phosphoproteins from human fibrosarcoma cells. Biochem. J. 350(Pt. 2):453–461.
  • Jiang, H. Y., Wek S. A., McGrath B. C., Lu D., Hai T., Harding H. P., Wang X., Ron D., Cavener D. R., and Wek R. C.. 2004. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol. Cell. Biol. 24:1365–1377.
  • Jonas, V., Lin C. R., Kawashima E., Semon D., Swanson L. W., Mermod J. J., Evans R. M., and Rosenfeld M. G.. 1985. Alternative RNA processing events in human calcitonin/calcitonin gene-related peptide gene expression. Proc. Natl. Acad. Sci. USA 82:1994–1998.
  • Kaufman, R. J. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13:1211–1233.
  • Koumenis, C., Naczki C., Koritzinsky M., Rastani S., Diehl A., Sonenberg N., Koromilas A., and Wouters B. G.. 2002. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2α. Mol. Cell. Biol. 22:7405–7416.
  • Kumar, R., Azam S., Sullivan J. M., Owen C., Cavener D. R., Zhang P., Ron D., Harding H. P., Chen J. J., Han A., White B. C., Krause G. S., and DeGracia D. J.. 2001. Brain ischemia and reperfusion activates the eukaryotic initiation factor 2alpha kinase, PERK. J. Neurochem. 77:1418–1421.
  • Kumar, R., Krause G. S., Yoshida H., Mori K., and DeGracia D. J.. 2003. Dysfunction of the unfolded protein response during global brain ischemia and reperfusion. J. Cereb. Blood Flow Metab. 23:462–471.
  • Lafeber, F. P., Hanssen R. G., Choy Y. M., Flik G., Herrmann-Erlee M. P., Pang P. K., and Bonga S. E.. 1988. Identification of hypocalcin (teleocalcin) isolated from trout Stannius corpuscles. Gen. Comp. Endocrinol. 69:19–30.
  • Lee, K., Tirasophon W., Shen X., Michalak M., Prywes R., Okada T., Yoshida H., Mori K., and Kaufman R. J.. 2002. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16:452–466.
  • Leonard, M. O., Cottell D. C., Godson C., Brady H. R., and Taylor C. T.. 2003. The role of HIF-1 alpha in transcriptional regulation of the proximal tubular epithelial cell response to hypoxia. J. Biol. Chem. 278:40296–40304.
  • Lin, P., Le-Niculescu H., Hofmeister R., McCaffery J. M., Jin M., Hennemann H., McQuistan T., De Vries L., and Farquhar M. G.. 1998. The mammalian calcium-binding protein, nucleobindin (Calnuc), is a Golgi resident protein. J. Cell Biol. 141:1515–1527.
  • Lin, P., Yao Y., Hofmeister R., Tsien R. Y., and Farquhar M. G.. 1999. Overexpression of CALNUC (nucleobindin) increases agonist and thapsigargin releasable Ca2+ storage in the Golgi. J. Cell Biol. 145:279–289.
  • Liu, C. Y., and Kaufman R. J.. 2003. The unfolded protein response. J. Cell Sci. 116:1861–1862.
  • Liu, D., Jia H., Holmes D. I., Stannard A., and Zachary I.. 2003. Vascular endothelial growth factor-regulated gene expression in endothelial cells: KDR-mediated induction of Egr3 and the related nuclear receptors Nur77, Nurr1, and Nor1. Arterioscler. Thromb. Vasc. Biol. 23:2002–2007.
  • Lockhart, D. J., Dong H., Byrne M. C., Follettie M. T., Gallo M. V., Chee M. S., Mittmann M., Wang C., Kobayashi M., Horton H., and Brown E. L.. 1996. Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat. Biotechnol. 14:1675–1680.
  • Longa, E. Z., Weinstein P. R., Carlson S., and Cummins R.. 1989. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84–91.
  • MacLennan, D. H., Brandl C. J., Korczak B., and Green N. M.. 1985. Amino-acid sequence of a Ca2+ + Mg2+-dependent ATPase from rabbit muscle sarcoplasmic reticulum, deduced from its complementary DNA sequence. Nature 316:696–700.
  • Mattson, M. P., LaFerla F. M., Chan S. L., Leissring M. A., Shepel P. N., and Geiger J. D.. 2000. Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 23:222–229.
  • McCudden, C. R., James K. A., Hasilo C., and 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.
  • Nakagawa, T., Zhu H., Morishima N., Li E., Xu J., Yankner B. A., and Yuan J.. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98–103.
  • Nishitoh, H., Matsuzawa A., Tobiume K., Saegusa K., Takeda K., Inoue K., Hori S., Kakizuka A., and Ichijo H.. 2002. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 16:1345–1355.
  • Okada, T., Yoshida H., Akazawa R., Negishi M., and Mori K.. 2002. Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem. J. 366:585–594.
  • Paschen, W., Aufenberg C., Hotop S., and Mengesdorf T.. 2003. Transient cerebral ischemia activates processing of xbp1 messenger RNA indicative of endoplasmic reticulum stress. J. Cereb. Blood Flow Metab. 23:449–461.
  • Paschen, W., and Frandsen A.. 2001. Endoplasmic reticulum dysfunction: a common denominator for cell injury in acute and degenerative diseases of the brain? J. Neurochem. 79:719–725.
  • Reimertz, C., Kogel D., Rami A., Chittenden T., and Prehn J. H.. 2003. Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J. Cell Biol. 162:587–597.
  • Reimold, A. M., Iwakoshi N. N., Manis J., Vallabhajosyula P., Szomolanyi-Tsuda E., Gravallese E. M., Friend D., Grusby M. J., Alt F., and Glimcher L. H.. 2001. Plasma cell differentiation requires the transcription factor XBP-1. Nature 412:300–307.
  • Rutkowski, D. T., and Kaufman R. J.. 2004. A trip to the ER: coping with stress. Trends Cell Biol. 14:20–28.
  • Sheikh-Hamad, D., Bick R., Wu G. Y., Christensen B. M., Razeghi P., Poindexter B., Taegtmeyer H., Wamsley A., Padda R., Entman M., Nielsen S., and Youker K.. 2003. Stanniocalcin-1 is a naturally occurring L-channel inhibitor in cardiomyocytes: relevance to human heart failure. Am. J. Physiol. Heart Circ. Physiol. 285:H442–H448.
  • Sheikh-Hamad, D., Rouse D., and Yang Y.. 2000. Regulation of stanniocalcin in MDCK cells by hypertonicity and extracellular calcium. Am. J. Physiol. Renal Physiol. 278:F417–F424.
  • Shen, J., Chen X., Hendershot L., and Prywes R.. 2002. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3:99–111.
  • Shen, X., Ellis R. E., Lee K., Liu C. Y., Yang K., Solomon A., Yoshida H., Morimoto R., Kurnit D. M., Mori K., and Kaufman R. J.. 2001. Complementary signaling pathways regulate the unfolded protein response and are required for Caenorhabditis elegans development. Cell 107:893–903.
  • Soto, C. 2003. Unfolding the role of protein misfolding in neurodegenerative diseases. Nat. Rev. Neurosci. 4:49–60.
  • Spector, D. L., Goldman R. D., and Leinwand L. A.. 1998. Culture and biochemical analysis of cells, p. 41.1–41.4. In Cells: a laboratory manual, vol. 1. Cold Spring Harbor Laboratory Press, New York, N.Y.
  • Sundell, K., Bjornsson B. T., Itoh H., and Kawauchi H.. 1992. Chum salmon (Oncorhynchus keta) stanniocalcin inhibits in vitro intestinal calcium uptake in Atlantic cod (Gadus morhua). J. Comp. Physiol. B 162:489–495.
  • Travers, K. J., Patil C. K., Wodicka L., Lockhart D. J., Weissman J. S., and Walter P.. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101:249–258.
  • Treiman, M. 2002. Regulation of the endoplasmic reticulum calcium storage during the unfolded protein response-significance in tissue ischemia? Trends Cardiovasc. Med. 12:57–62.
  • Urano, F., Bertolotti A., and Ron D.. 2000. IRE1 and efferent signaling from the endoplasmic reticulum. J. Cell Sci. 113(Pt. 21):3697–3702.
  • van Rossum, D., Hanisch U. K., and Quirion R.. 1997. Neuroanatomical localization, pharmacological characterization and functions of CGRP, related peptides, and their receptors. Neurosci. Biobehav. Rev. 21:649–678.
  • Wagner, G. F. 1994. The molecular biology of the corpuscles of stannius and regulation of stanniocalcin gene expression, p. 273–306. In Hew C. (ed.), Fish physiology, vol. 13. Academic Press, Inc., New York, N.Y.
  • Wagner, G. F., Hampong M., Park C. M., and Copp D. H.. 1986. Purification, characterization, and bioassay of teleocalcin, a glycoprotein from salmon corpuscles of Stannius. Gen. Comp. Endocrinol. 63:481–491.
  • Wagner, G. F., Vozzolo B. L., Jaworski E., Haddad M., Kline R. L., Olsen H. S., Rosen C. A., Davidson M. B., and Renfro J. L.. 1997. Human stanniocalcin inhibits renal phosphate excretion in the rat. J. Bone Miner. Res. 12:165–171.
  • Wary, K. K., Thakker G. D., Humtsoe J. O., and Yang J.. 2003. Analysis of VEGF-responsive genes involved in the activation of endothelial cells. Mol. Cancer 2:25.
  • Ye, J., Rawson R. B., Komuro R., Chen X., Dave U. P., Prywes R., Brown M. S., and Goldstein J. L.. 2000. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6:1355–1364.
  • Yoshida, H., Matsui T., Yamamoto A., Okada T., and Mori K.. 2001. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881–891.
  • Zhang, K., Lindsberg P. J., Tatlisumak T., Kaste M., Olsen H. S., and Andersson L. C.. 2000. Stanniocalcin: a molecular guard of neurons during cerebral ischemia. Proc. Natl. Acad. Sci. USA 97:3637–3642.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.