Real-time Detection and Continuous Monitoring of ER Stress in Vitro and in Vivo by ES-TRAP: Evidence for Systemic, Transient ER Stress During Endotoxemia

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2006 Aug 1

PMID 16877567

Citations 32

Authors

Nobuhiko Hiramatsu

Ayumi Kasai

Kunihiro Hayakawa

Jian Yao

Masanori Kitamura

Affiliations

Soon will be listed here.

Abstract

Activity of secreted alkaline phosphatase (SEAP) produced by transfected cells is rapidly down-regulated by endoplasmic reticulum (ER) stress independent of transcriptional regulation. This phenomenon was observed in a wide range of cell types triggered by various ER stress inducers. The magnitude of the decrease in SEAP was proportional to the extent of ER stress and inversely correlated with the induction of endogenous ER stress markers grp78 and grp94. In contrast to SEAP, activity of secreted luciferase was less susceptible to ER stress. The decrease in SEAP activity by ER stress was caused by abnormal post-translational modification, accelerated degradation and reduced secretion of SEAP protein. In transgenic mice constitutively producing SEAP, systemic induction of ER stress led to reduction in serum SEAP. In these mice, administration with lipopolysaccharide caused rapid, transient decrease in serum SEAP activity, and it was correlated with up-regulation of grp78 in several organs including the spleen, lung, kidney, liver and heart. These results elucidated for the first time a possible involvement of transient, systemic ER stress in endotoxemia and provided evidence for usefulness of ER stress responsive alkaline phosphatase for real-time monitoring of ER stress in vitro and in vivo.

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References

Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner B . Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature. 2000; 403(6765):98-103. DOI: 10.1038/47513. View

Yamauchi K, Takano Y, Kasai A, Hayakawa K, Hiramatsu N, Enomoto N . Screening and identification of substances that regulate nephrin gene expression using engineered reporter podocytes. Kidney Int. 2006; 70(5):892-900. DOI: 10.1038/sj.ki.5001625. View

Lee A . The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci. 2001; 26(8):504-10. DOI: 10.1016/s0968-0004(01)01908-9. View

Katayama T, Imaizumi K, Honda A, Yoneda T, Kudo T, Takeda M . Disturbed activation of endoplasmic reticulum stress transducers by familial Alzheimer's disease-linked presenilin-1 mutations. J Biol Chem. 2001; 276(46):43446-54. DOI: 10.1074/jbc.M104096200. View

Schlatter S, Rimann M, Kelm J, Fussenegger M . SAMY, a novel mammalian reporter gene derived from Bacillus stearothermophilus alpha-amylase. Gene. 2002; 282(1-2):19-31. DOI: 10.1016/s0378-1119(01)00824-1. View

Tashiro M, Ernst S, Edwards J, Williams J . Hyperthermia induces multiple pancreatic heat shock proteins and protects against subsequent arginine-induced acute pancreatitis in rats. Digestion. 2002; 65(2):118-26. DOI: 10.1159/000057713. View

Taxis C, Vogel F, Wolf D . ER-golgi traffic is a prerequisite for efficient ER degradation. Mol Biol Cell. 2002; 13(6):1806-18. PMC: 117605. DOI: 10.1091/mbc.01-08-0399. View

Iwawaki T, Akai R, Kohno K, Miura M . A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat Med. 2004; 10(1):98-102. DOI: 10.1038/nm970. View

Markova S, Golz S, Frank L, Kalthof B, Vysotski E . Cloning and expression of cDNA for a luciferase from the marine copepod Metridia longa. A novel secreted bioluminescent reporter enzyme. J Biol Chem. 2003; 279(5):3212-7. DOI: 10.1074/jbc.M309639200. View

10.

Kondoh M, Tsukada M, Kuronaga M, Higashimoto M, Takiguchi M, Himeno S . Induction of hepatic metallothionein synthesis by endoplasmic reticulum stress in mice. Toxicol Lett. 2004; 148(1-2):133-9. DOI: 10.1016/j.toxlet.2003.12.066. View

11.

Mao C, Dong D, Little E, Luo S, Lee A . Transgenic mouse model for monitoring endoplasmic reticulum stress in vivo. Nat Med. 2004; 10(10):1013-4. DOI: 10.1038/nm1004-1013. View

12.

Nakagomi T, Kitada O, Kuribayashi K, Yoshikawa H, Ozawa K, Ogawa S . The 150-kilodalton oxygen-regulated protein ameliorates lipopolysaccharide-induced acute lung injury in mice. Am J Pathol. 2004; 165(4):1279-88. PMC: 1618642. DOI: 10.1016/S0002-9440(10)63387-1. View

13.

Kozutsumi Y, Segal M, Normington K, Gething M, Sambrook J . The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature. 1988; 332(6163):462-4. DOI: 10.1038/332462a0. View

14.

Berger J, HAUBER J, Hauber R, Geiger R, Cullen B . Secreted placental alkaline phosphatase: a powerful new quantitative indicator of gene expression in eukaryotic cells. Gene. 1988; 66(1):1-10. DOI: 10.1016/0378-1119(88)90219-3. View

15.

Derman A, Beckwith J . Escherichia coli alkaline phosphatase fails to acquire disulfide bonds when retained in the cytoplasm. J Bacteriol. 1991; 173(23):7719-22. PMC: 212545. DOI: 10.1128/jb.173.23.7719-7722.1991. View

16.

Cullen B, Malim M . Secreted placental alkaline phosphatase as a eukaryotic reporter gene. Methods Enzymol. 1992; 216:362-8. DOI: 10.1016/0076-6879(92)16033-g. View

17.

Kitamura M, Taylor S, Unwin R, Burton S, Shimizu F, Fine L . Gene transfer into the rat renal glomerulus via a mesangial cell vector: site-specific delivery, in situ amplification, and sustained expression of an exogenous gene in vivo. J Clin Invest. 1994; 94(2):497-505. PMC: 296122. DOI: 10.1172/JCI117361. View

18.

Kitamura M, Suto T, Yokoo T, Shimizu F, Fine L . Transforming growth factor-beta 1 is the predominant paracrine inhibitor of macrophage cytokine synthesis produced by glomerular mesangial cells . J Immunol. 1996; 156(8):2964-71. View

19.

Ishiyama M, Tominaga H, Shiga M, Sasamoto K, Ohkura Y, Ueno K . A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet. Biol Pharm Bull. 1996; 19(11):1518-20. DOI: 10.1248/bpb.19.1518. View

20.

Sone M, Kishigami S, Yoshihisa T, Ito K . Roles of disulfide bonds in bacterial alkaline phosphatase. J Biol Chem. 1997; 272(10):6174-8. DOI: 10.1074/jbc.272.10.6174. View