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Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

The Expression of the Cold Shock Protein RNA Binding Motif Protein 3 is Transcriptionally Responsive to Organ Temperature in Mice

Author(s): Ayako Ushio and Ko Eto*

Volume 28, Issue 3, 2021

Published on: 24 September, 2020

Page: [270 - 275] Pages: 6

DOI: 10.2174/0929866527666200924144424

Price: $65

Abstract

Background: Mild hypothermia, i.e. maintenance of organ temperature by up to 8°C lower than body temperature, is a critical strategy for exerting some functions of the cells and organs normally, and is an useful therapy for recovering properly from some diseases, including myocardial infarction, cardiac arrest, brain injury, and ischemic stroke. Nevertheless, there were no focusses so far on organ temperature and potential responses of gene expression to organ temperature in organs of homeothermic animals that survive under normal conditions.

Objective: The present study aimed to assess organ temperature in homeothermic animals and evaluate the effect of their organ temperature on the expression of the cold shock protein RNA binding motif protein 3 (RBM3), and to gain insights into the organ temperature-mediated regulation of RBM3 gene transcription via Nuclear factor β-light-chain-enhancer of activated B cells (NF-κB) p65, which had been identified as a transcription factor that is activated by undergoing the Ser276 phosphorylation and promotes the RBM3 gene expression during mild hypothermia.

Methods: We measured the temperature of several organs, where RBM3 expression was examined, in female and male mice. Next, in male mice, we tested NF-κB p65 expression and its Ser276 phosphorylation in organs that have their lower temperature than body temperature and compared them with those in organs that have their temperature near body temperature.

Results: Organ temperature was around 32°C in the brain and reproductive organs, which is lower than the body temperature, and around 37°C in the heart, liver, and kidney, which is comparable to the body temperature. The expression of RBM3 was detected greatly in the brain and reproductive organs with their organ temperature of around 32°C, and poorly in the heart, liver, and kidney with their organ temperature of around 37°C. In accordance with the changes in the RBM3 expression, the NF-κB p65 Ser276 phosphorylation was detected more greatly in the testis and brain with their organ temperature of around 32°C, than in the heart, liver, and kidney with their organ temperature of around 37°C, although the NF-κB p65 expression was unchanged among all the organs tested.

Discussion: Our data suggested that organ temperature lower than body temperature causes the expression of RBM3 in the brain and reproductive organs of mice, and that lower organ temperature causes the NF-κB p65 activation through the Ser276 phosphorylation, resulting in an increase in the RBM3 gene transcription, in the brain and reproductive organs of mice.

Conclusion: The study may present the possibility that organ temperature-induced alterations in gene expression are organ specific in homeotherms and the possibility that organ temperature-induced alterations in gene expression are transcriptionally regulated in some organs of homeotherms.

Keywords: Organ temperature, cold signal, mild hypothermia, cold shock protein, RNA-binding protein, RBM3, transcription factor, NF-κB p65, hypothermic animal.

Graphical Abstract
[1]
Jiang, J.Y.; Xu, W.; Li, W.P.; Gao, G.Y.; Bao, Y.H.; Liang, Y.M.; Luo, Q.Z. Effect of long-term mild hypothermia or short-term mild hypothermia on outcome of patients with severe traumatic brain injury. J. Cereb. Blood Flow Metab., 2006, 26(6), 771-776.
[http://dx.doi.org/10.1038/sj.jcbfm.9600253] [PMID: 16306933]
[2]
Mottillo, S.; Sharma, K.; Eisenberg, M.J. Therapeutic hypothermia in acute myocardial infarction: a systematic review. Can. J. Cardiol., 2011, 27(5), 555-561.
[http://dx.doi.org/10.1016/j.cjca.2010.12.027] [PMID: 21641172]
[3]
England, T.N. Hypothermia after cardiac arrest study group. Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N. Engl. J. Med., 2002, 346(8), 549-556.
[http://dx.doi.org/10.1056/NEJMoa012689] [PMID: 11856793]
[4]
Hong, J.M.; Lee, J.S.; Song, H.J.; Jeong, H.S.; Choi, H.A.; Lee, K. Therapeutic hypothermia after recanalization in patients with acute ischemic stroke. Stroke, 2014, 45(1), 134-140.
[http://dx.doi.org/10.1161/STROKEAHA.113.003143] [PMID: 24203846]
[5]
Sonna, L.A.; Fujita, J.; Gaffin, S.L.; Lilly, C.M. Invited review: effects of heat and cold stress on mammalian gene expression. J. Appl. Physiol., 2002, 92(4), 1725-1742.
[http://dx.doi.org/10.1152/japplphysiol.01143.2001] [PMID: 11896043]
[6]
Ushio, A.; Eto, K. RBM3 expression is upregulated by NF-κB p65 activity, protecting cells from apoptosis, during mild hypothermia. J. Cell. Biochem., 2018, 119(7), 5734-5749.
[http://dx.doi.org/10.1002/jcb.26757] [PMID: 29388696]
[7]
Danno, S.; Nishiyama, H.; Higashitsuji, H.; Yokoi, H.; Xue, J.H.; Itoh, K.; Matsuda, T.; Fujita, J. Increased transcript level of RBM3, a member of the glycine-rich RNA-binding protein family, in human cells in response to cold stress. Biochem. Biophys. Res. Commun., 1997, 236(3), 804-807.
[http://dx.doi.org/10.1006/bbrc.1997.7059] [PMID: 9245737]
[8]
Al-Fageeh, M.B.; Smales, C.M. Control and regulation of the cellular responses to cold shock: the responses in yeast and mammalian systems. Biochem. J., 2006, 397(2), 247-259.
[http://dx.doi.org/10.1042/BJ20060166] [PMID: 16792527]
[9]
Wellmann, S.; Bührer, C.; Moderegger, E.; Zelmer, A.; Kirschner, R.; Koehne, P.; Fujita, J.; Seeger, K. Oxygen-regulated expression of the RNA-binding proteins RBM3 and CIRP by a HIF-1-independent mechanism. J. Cell Sci., 2004, 117(Pt 9), 1785-1794.
[http://dx.doi.org/10.1242/jcs.01026] [PMID: 15075239]
[10]
Sureban, S.M.; Ramalingam, S.; Natarajan, G.; May, R.; Subramaniam, D.; Bishnupuri, K.S.; Morrison, A.R.; Dieckgraefe, B.K.; Brackett, D.J.; Postier, R.G.; Houchen, C.W.; Anant, S. Translation regulatory factor RBM3 is a proto-oncogene that prevents mitotic catastrophe. Oncogene, 2008, 27(33), 4544-4556.
[http://dx.doi.org/10.1038/onc.2008.97] [PMID: 18427544]
[11]
Wellmann, S.; Truss, M.; Bruder, E.; Tornillo, L.; Zelmer, A.; Seeger, K.; Bührer, C. The RNA-binding protein RBM3 is required for cell proliferation and protects against serum deprivation-induced cell death. Pediatr. Res., 2010, 67(1), 35-41.
[http://dx.doi.org/10.1203/PDR.0b013e3181c13326] [PMID: 19770690]
[12]
Lleonart, M.E. A new generation of proto-oncogenes: cold-inducible RNA binding proteins. Biochim. Biophys. Acta, 2010, 1805(1), 43-52.
[PMID: 19900510]
[13]
Derry, J.M.; Kerns, J.A.; Francke, U. RBM3, a novel human gene in Xp11.23 with a putative RNA-binding domain. Hum. Mol. Genet., 1995, 4(12), 2307-2311.
[http://dx.doi.org/10.1093/hmg/4.12.2307] [PMID: 8634703]
[14]
Nishiyama, H.; Higashitsuji, H.; Yokoi, H.; Itoh, K.; Danno, S.; Matsuda, T.; Fujita, J. Cloning and characterization of human CIRP (cold-inducible RNA-binding protein) cDNA and chromosomal assignment of the gene. Gene, 1997, 204(1-2), 115-120.
[http://dx.doi.org/10.1016/S0378-1119(97)00530-1] [PMID: 9434172]
[15]
Uochi, T.; Asashima, M. XCIRP (Xenopus homolog of cold-inducible RNA-binding protein) is expressed transiently in developing pronephros and neural tissue. Gene, 1998, 211(2), 245-250.
[http://dx.doi.org/10.1016/S0378-1119(98)00102-4] [PMID: 9602141]
[16]
Bhatia, R.; Dube, D.K.; Gaur, A.; Robertson, D.R.; Lemanski, S.L.; McLean, M.D.; Lemanski, L.F. Expression of axolotl RNA-binding protein during development of the Mexican axolotl. Cell Tissue Res., 1999, 297(2), 283-290.
[http://dx.doi.org/10.1007/s004410051356] [PMID: 10470498]
[17]
Danno, S.; Itoh, K.; Matsuda, T.; Fujita, J. Decreased expression of mouse Rbm3, a cold-shock protein, in Sertoli cells of cryptorchid testis. Am. J. Pathol., 2000, 156(5), 1685-1692.
[http://dx.doi.org/10.1016/S0002-9440(10)65039-0] [PMID: 10793079]
[18]
Matsumoto, K.; Aoki, K.; Dohmae, N.; Takio, K.; Tsujimoto, M. CIRP2, a major cytoplasmic RNA-binding protein in Xenopus oocytes. Nucleic Acids Res., 2000, 28(23), 4689-4697.
[http://dx.doi.org/10.1093/nar/28.23.4689] [PMID: 11095679]
[19]
Eto, K.; Eda, K.; Hayano, M.; Goto, S.; Nagao, K.; Kawasaki, T.; Kashimura, H.; Tarui, H.; Nishimura, O.; Agata, K.; Abe, S. Reduced expression of an RNA-binding protein by prolactin leads to translational silencing of programmed cell death protein 4 and apoptosis in newt spermatogonia. J. Biol. Chem., 2009, 284(35), 23260-23271.
[http://dx.doi.org/10.1074/jbc.M109.018622] [PMID: 19556246]
[20]
Graumann, P.L.; Marahiel, M.A. A superfamily of proteins that contain the cold-shock domain. Trends Biochem. Sci., 1998, 23(8), 286-290.
[http://dx.doi.org/10.1016/S0968-0004(98)01255-9] [PMID: 9757828]
[21]
Gualerzi, C.O.; Giuliodori, A.M.; Pon, C.L. Transcriptional and post-transcriptional control of cold-shock genes. J. Mol. Biol., 2003, 331(3), 527-539.
[http://dx.doi.org/10.1016/S0022-2836(03)00732-0] [PMID: 12899826]
[22]
Phadtare, S.; Alsina, J.; Inouye, M. Cold-shock response and cold-shock proteins. Curr. Opin. Microbiol., 1999, 2(2), 175-180.
[http://dx.doi.org/10.1016/S1369-5274(99)80031-9] [PMID: 10322168]
[23]
Dresios, J.; Aschrafi, A.; Owens, G.C.; Vanderklish, P.W.; Edelman, G.M.; Mauro, V.P. Cold stress-induced protein Rbm3 binds 60S ribosomal subunits, alters microRNA levels, and enhances global protein synthesis. Proc. Natl. Acad. Sci. USA, 2005, 102(6), 1865-1870.
[http://dx.doi.org/10.1073/pnas.0409764102] [PMID: 15684048]
[24]
Smart, F.; Aschrafi, A.; Atkins, A.; Owens, G.C.; Pilotte, J.; Cunningham, B.A.; Vanderklish, P.W. Two isoforms of the cold-inducible mRNA-binding protein RBM3 localize to dendrites and promote translation. J. Neurochem., 2007, 101(5), 1367-1379.
[http://dx.doi.org/10.1111/j.1471-4159.2007.04521.x] [PMID: 17403028]
[25]
Chip, S.; Zelmer, A.; Ogunshola, O.O.; Felderhoff-Mueser, U.; Nitsch, C.; Bührer, C.; Wellmann, S. The RNA-binding protein RBM3 is involved in hypothermia induced neuroprotection. Neurobiol. Dis., 2011, 43(2), 388-396.
[http://dx.doi.org/10.1016/j.nbd.2011.04.010] [PMID: 21527344]
[26]
Zeng, Y.; Kulkarni, P.; Inoue, T.; Getzenberg, R.H. Down-regulating cold shock protein genes impairs cancer cell survival and enhances chemosensitivity. J. Cell. Biochem., 2009, 107(1), 179-188.
[http://dx.doi.org/10.1002/jcb.22114] [PMID: 19277990]
[27]
Kita, H.; Carmichael, J.; Swartz, J.; Muro, S.; Wyttenbach, A.; Matsubara, K.; Rubinsztein, D.C.; Kato, K. Modulation of polyglutamine-induced cell death by genes identified by expression profiling. Hum. Mol. Genet., 2002, 11(19), 2279-2287.
[http://dx.doi.org/10.1093/hmg/11.19.2279] [PMID: 12217956]
[28]
Nagashima, K.; Nakai, S.; Tanaka, M.; Kanosue, K. Neuronal circuitries involved in thermoregulation. Auton. Neurosci., 2000, 85(1-3), 18-25.
[http://dx.doi.org/10.1016/S1566-0702(00)00216-2] [PMID: 11189023]

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