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Protein & Peptide Letters

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

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Mini-Review Article

Cold-Induced RNA-Binding Protein and RNA-Binding Motif Protein 3: Two RNA Molecular Chaperones Closely Related to Reproductive Development and Reproductive System Diseases

Author(s): Jiahao Liu, Qinqin Wei, Yingji Jin, Yuji Jin* and Yong Jiang*

Volume 30, Issue 1, 2023

Published on: 19 December, 2022

Page: [2 - 12] Pages: 11

DOI: 10.2174/0929866530666221124122507

Price: $65

Abstract

Cold-induced RNA-binding protein (CIRP) and RNA-binding motif protein 3 (RBM3) have recently been reported to be involved in cold stress in mammals. These proteins are expressed at low levels in various normal cells, tissues, and organs but can be upregulated upon stimulation by multiple stressors. Studies have shown that CIRP and RBM3 are multifunctional RNA molecular chaperones with different biological functions in various physiological and pathophysiological processes, such as reproductive development, the inflammatory response, the immune response, nerve injury regulation, and tumorigenesis. This paper reviews recent studies on the structure, localization and correlation of CIRP and RBM3 with reproductive development and reproductive system diseases.

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[1]
Fornace, A.J., Jr; Alamo, I., Jr; Hollander, M.C. DNA damage-inducible transcripts in mammalian cells. Proc. Natl. Acad. Sci. USA, 1988, 85(23), 8800-8804.
[http://dx.doi.org/10.1073/pnas.85.23.8800] [PMID: 3194391]
[2]
Derry, J.M.J.; 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]
[3]
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]
[4]
Ciuzan, O.; Hancock, J.; Pamfil, D.; Wilson, I.; Ladomery, M. The evolutionarily conserved multifunctional glycine-rich RNA-binding proteins play key roles in development and stress adaptation. Physiol. Plant., 2015, 153(1), 1-11.
[http://dx.doi.org/10.1111/ppl.12286] [PMID: 25243592]
[5]
Nishiyama, H.; Danno, S.; Kaneko, Y.; Itoh, K.; Yokoi, H.; Fukumoto, M.; Okuno, H.; Millán, J.L.; Matsuda, T.; Yoshida, O.; Fujita, J. Decreased expression of cold-inducible RNA-binding protein (CIRP) in male germ cells at elevated temperature. Am. J. Pathol., 1998, 152(1), 289-296.
[PMID: 9422546]
[6]
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]
[7]
Al-Fageeh, M.B.; Smales, C.M. Cold-inducible RNA binding protein (CIRP) expression is modulated by alternative mRNAs. RNA, 2009, 15(6), 1164-1176.
[http://dx.doi.org/10.1261/rna.1179109] [PMID: 19398494]
[8]
Liao, Y.; Tong, L.; Tang, L.; Wu, S. The role of cold‐inducible RNA binding protein in cell stress response. Int. J. Cancer, 2017, 141(11), 2164-2173.
[http://dx.doi.org/10.1002/ijc.30833] [PMID: 28608439]
[9]
Zhong, P.; Peng, J.; Bian, Z.; Huang, H. The role of cold inducible RNA-binding protein in cardiac physiology and diseases. Front. Pharmacol., 2021, 12, 610792.
[http://dx.doi.org/10.3389/fphar.2021.610792] [PMID: 33716740]
[10]
Matsuda, A.; Ogawa, M.; Yanai, H.; Naka, D.; Goto, A.; Ao, T.; Tanno, Y.; Takeda, K.; Watanabe, Y.; Honda, K.; Taniguchi, T. Generation of mice deficient in RNA-binding motif protein 3 (RBM3) and characterization of its role in innate immune responses and cell growth. Biochem. Biophys. Res. Commun., 2011, 411(1), 7-13.
[http://dx.doi.org/10.1016/j.bbrc.2011.06.038] [PMID: 21684257]
[11]
Adler, D.; Lindstrot, A.; Ochsenfahrt, J.; Fuchs, K.; Wernert, N. Epigenetics-related genes in prostate cancer: Expression profile in prostate cancer tissues, androgen-sensitive and insensitive cell lines. Int. J. Mol. Med., 2013, 31(1), 21-25.
[PMID: 23135352]
[12]
Liao, Y.; Feng, J.; Zhang, Y.; Tang, L.; Wu, S. The mechanism of CIRP in inhibition of keratinocytes growth arrest and apoptosis following low dose UVB radiation. Mol. Carcinog., 2017, 56(6), 1554-1569.
[http://dx.doi.org/10.1002/mc.22597] [PMID: 27864909]
[13]
Tan, Y.L.; Tey, S.M.; Ho, H.K. Moderate hypothermia effectively alleviates acetaminophen-induced liver injury with prolonged action beyond cooling. Dose Response, 2020, 18(4), 1559325820970846.
[http://dx.doi.org/10.1177/1559325820970846] [PMID: 33239997]
[14]
Roilo, M.; Kullmann, M.K.; Hengst, L. Cold-inducible RNA-binding protein (CIRP) induces translation of the cell-cycle inhibitor p27Kip1. Nucleic Acids Res., 2018, 46(6), 3198-3210.
[http://dx.doi.org/10.1093/nar/gkx1317] [PMID: 29361038]
[15]
Liu, Y.; Liu, P.; Hu, Y.; Cao, Y.; Lu, J.; Yang, Y.; Lv, H.; Lian, S.; Xu, B.; Li, S. Cold-induced RNA-binding protein promotes glucose metabolism and reduces apoptosis by increasing AKT phosphorylation in mouse skeletal muscle under acute cold exposure. Front. Mol. Biosci., 2021, 8, 685993.
[http://dx.doi.org/10.3389/fmolb.2021.685993] [PMID: 34395524]
[16]
Zhu, X.; Bührer, C.; Wellmann, S. Cold-inducible proteins CIRP and RBM3, a unique couple with activities far beyond the cold. Cell. Mol. Life Sci., 2016, 73(20), 3839-3859.
[http://dx.doi.org/10.1007/s00018-016-2253-7] [PMID: 27147467]
[17]
Xia, Z.; Zheng, X.; Zheng, H.; Liu, X.; Yang, Z.; Wang, X. Cold-inducible RNA-binding protein (CIRP) regulates target mRNA stabilization in the mouse testis. FEBS Lett., 2012, 586(19), 3299-3308.
[http://dx.doi.org/10.1016/j.febslet.2012.07.004] [PMID: 22819822]
[18]
Aziz, M.; Brenner, M.; Wang, P. Extracellular CIRP (eCIRP) and inflammation. J. Leukoc. Biol., 2019, 106(1), 133-146.
[http://dx.doi.org/10.1002/JLB.3MIR1118-443R] [PMID: 30645013]
[19]
Lujan, D.A.; Ochoa, J.L.; Hartley, R.S. Cold‐inducible RNA binding protein in cancer and inflammation. Wiley Interdiscip. Rev. RNA, 2018, 9(2), 1462.
[http://dx.doi.org/10.1002/wrna.1462] [PMID: 29322631]
[20]
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]
[21]
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]
[22]
Tang, C.; Wang, Y.; Lan, D.; Feng, X.; Zhu, X.; Nie, P.; Yue, H. Analysis of gene expression profiles reveals the regulatory network of cold-inducible RNA-binding protein mediating the growth of BHK-21 cells. Cell Biol. Int., 2015, 39(6), 678-689.
[http://dx.doi.org/10.1002/cbin.10438] [PMID: 25597958]
[23]
Pereira, B.; Billaud, M.; Almeida, R. RNA-binding proteins in cancer: Old players and new actors. Trends Cancer, 2017, 3(7), 506-528.
[http://dx.doi.org/10.1016/j.trecan.2017.05.003] [PMID: 28718405]
[24]
Chaikam, V.; Karlson, D.T. Comparison of structure, function and regulation of plant cold shock domain proteins to bacterial and animal cold shock domain proteins. BMB Rep., 2010, 43(1), 1-8.
[http://dx.doi.org/10.5483/BMBRep.2010.43.1.001] [PMID: 20132728]
[25]
Mangeon, A.; Junqueira, R.M.; Sachetto-Martins, G. Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal. Behav., 2010, 5(2), 99-104.
[http://dx.doi.org/10.4161/psb.5.2.10336] [PMID: 20009520]
[26]
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]
[27]
Nishiyama, H.; Xue, J.H.; Sato, T.; Fukuyama, H.; Mizuno, N.; Houtani, T.; Sugimoto, T.; Fujita, J. Diurnal change of the cold-inducible RNA-binding protein (CIRP) expression in mouse brain. Biochem. Biophys. Res. Commun., 1998, 245(2), 534-538.
[http://dx.doi.org/10.1006/bbrc.1998.8482] [PMID: 9571190]
[28]
Chen, L.; Tian, Q.; Wang, W. Association between CIRP expression and hypoxic ischemic brain injury in neonatal rats. Exp. Ther. Med., 2019, 18(3), 1515-1520.
[http://dx.doi.org/10.3892/etm.2019.7767] [PMID: 31410103]
[29]
Sugimoto, K.; Jiang, H. Cold stress and light signals induce the expression of cold-inducible RNA binding protein (CIRP) in the brain and eye of the Japanese treefrog (Hyla japonica). Comp. Biochem. Physiol. A Mol. Integr. Physiol., 2008, 151(4), 628-636.
[http://dx.doi.org/10.1016/j.cbpa.2008.07.027] [PMID: 18722545]
[30]
Tong, G.; Endersfelder, S.; Rosenthal, L.M.; Wollersheim, S.; Sauer, I.M.; Bührer, C.; Berger, F.; Schmitt, K.R.L. Effects of moderate and deep hypothermia on RNA-binding proteins RBM3 and CIRP expressions in murine hippocampal brain slices. Brain Res., 2013, 1504, 74-84.
[http://dx.doi.org/10.1016/j.brainres.2013.01.041] [PMID: 23415676]
[31]
Kaneko, T.; Kibayashi, K. Mild hypothermia facilitates the expression of cold-inducible RNA-binding protein and heat shock protein 70.1 in mouse brain. Brain Res., 2012, 1466, 128-136.
[http://dx.doi.org/10.1016/j.brainres.2012.05.001] [PMID: 22609236]
[32]
Zhou, K.; Cui, S.; Duan, W.; Zhang, J.; Huang, J.; Wang, L.; Gong, Z.; Zhou, Y. Cold‐inducible RNA‐binding protein contributes to intracerebral hemorrhage‐induced brain injury via TLR4 signaling. Brain Behav., 2020, 10(6), e01618.
[http://dx.doi.org/10.1002/brb3.1618] [PMID: 32285591]
[33]
Chen, M.; Fu, H.; Zhang, J.; Huang, H.; Zhong, P. CIRP downregulation renders cardiac cells prone to apoptosis in heart failure. Biochem. Biophys. Res. Commun., 2019, 517(4), 545-550.
[http://dx.doi.org/10.1016/j.bbrc.2019.05.012] [PMID: 31405566]
[34]
Xu, Q.; Wang, M.; Guo, H.; Liu, H.; Zhang, G.; Xu, C.; Chen, H. Emodin alleviates severe acute pancreatitis-associated acute lung injury by inhibiting the cold-inducible RNA-binding protein (CIRP)-mediated activation of the NLRP3/IL-1β/CXCL1 signaling. Front. Pharmacol., 2021, 12, 655372.
[http://dx.doi.org/10.3389/fphar.2021.655372] [PMID: 33967799]
[35]
Liu, P.; Yao, R.; Shi, H.; Liu, Y.; Lian, S.; Yang, Y.; Yang, H.; Li, S. Effects of cold-inducible RNA-binding protein (CIRP) on liver glycolysis during acute cold exposure in C57BL/6 mice. Int. J. Mol. Sci., 2019, 20(6), 1470.
[http://dx.doi.org/10.3390/ijms20061470] [PMID: 30909542]
[36]
Higashitsuji, H.; Fujita, T.; Higashitsuji, H.; Fujita, J. Mammalian cold-inducible RNA-binding protein facilitates wound healing through activation of AMP-activated protein kinase. Biochem. Biophys. Res. Commun., 2020, 533(4), 1191-1197.
[http://dx.doi.org/10.1016/j.bbrc.2020.10.004] [PMID: 33041006]
[37]
Liu, W.; Yan, Y.; Han, D.; Li, Y.; Wang, Q.; Li, J.; Liu, F.; Zheng, X. CIRP secretion during cardiopulmonary bypass is associated with increased risk of postoperative acute kidney injury. Thorac. Cardiovasc. Surg., 2021, 69(6), 542-547.
[http://dx.doi.org/10.1055/s-0041-1730450] [PMID: 34233365]
[38]
Li, Y.; Wu, X.; Miao, S.; Cao, Q. MiR-383-5p promotes apoptosis of ovarian granulosa cells by targeting CIRP through the PI3K/AKT signaling pathway. Arch. Gynecol. Obstet., 2022, 306(2), 501-512.
[http://dx.doi.org/10.1007/s00404-022-06461-z] [PMID: 35226160]
[39]
Wang, X.; Liu, Z.; Ma, A. Interpretation of the genotype by tissue interactions of four genes (AFP1, CIRP, YB-1, and HMGB1) in Takifugu rubripes under different low-temperature conditions. Front. Mol. Biosci., 2022, 9, 897935.
[http://dx.doi.org/10.3389/fmolb.2022.897935] [PMID: 35847974]
[40]
Jackson, T.C.; Janesko-Feldman, K.; Carlson, S.W.; Kotermanski, S.E.; Kochanek, P.M. Robust RBM3 and β-klotho expression in developing neurons in the human brain. J. Cereb. Blood Flow Metab., 2019, 39(12), 2355-2367.
[http://dx.doi.org/10.1177/0271678X19878889] [PMID: 31566073]
[41]
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]
[42]
Pilotte, J.; Cunningham, B.A.; Edelman, G.M.; Vanderklish, P.W. Developmentally regulated expression of the cold-inducible RNA-binding motif protein 3 in euthermic rat brain. Brain Res., 2009, 1258, 12-24.
[http://dx.doi.org/10.1016/j.brainres.2008.12.050] [PMID: 19150436]
[43]
Larrayoz, I.M.; Rey-Funes, M.; Contartese, D.S.; Rolón, F.; Sarotto, A.; Dorfman, V.B.; Loidl, C.F.; Martínez, A. Cold shock proteins are expressed in the retina following exposure to low temperatures. PLoS One, 2016, 11(8), e0161458.
[http://dx.doi.org/10.1371/journal.pone.0161458] [PMID: 27556928]
[44]
Trollmann, R.; Rehrauer, H.; Schneider, C.; Krischke, G.; Huemmler, N.; Keller, S.; Rascher, W.; Gassmann, M. Late-gestational systemic hypoxia leads to a similar early gene response in mouse placenta and developing brain. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2010, 299(6), R1489-R1499.
[http://dx.doi.org/10.1152/ajpregu.00697.2009] [PMID: 20926767]
[45]
Jo, J.W.; Jee, B.C.; Suh, C.S.; Kim, S.H. The beneficial effects of antifreeze proteins in the vitrification of immature mouse oocytes. PLoS One, 2012, 7(5), e37043.
[http://dx.doi.org/10.1371/journal.pone.0037043] [PMID: 22649508]
[46]
Zhu, X.; Zelmer, A.; Kapfhammer, J.P.; Wellmann, S. Cold‐inducible RBM3 inhibits PERK phosphorylation through cooperation with NF90 to protect cells from endoplasmic reticulum stress. FASEB J., 2016, 30(2), 624-634.
[http://dx.doi.org/10.1096/fj.15-274639] [PMID: 26472337]
[47]
Zhong, P.; Huang, H. Recent progress in the research of cold-inducible RNA-binding protein. Future Sci. OA, 2017, 3(4), FSO246.
[http://dx.doi.org/10.4155/fsoa-2017-0077] [PMID: 29134130]
[48]
De Leeuw, F.; Zhang, T.; Wauquier, C.; Huez, G.; Kruys, V.; Gueydan, C. The cold-inducible RNA-binding protein migrates from the nucleus to cytoplasmic stress granules by a methylation-dependent mechanism and acts as a translational repressor. Exp. Cell Res., 2007, 313(20), 4130-4144.
[http://dx.doi.org/10.1016/j.yexcr.2007.09.017] [PMID: 17967451]
[49]
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]
[50]
Al-Astal, H.I.; Massad, M.; AlMatar, M.; Ekal, H. Cellular functions of RNA-binding motif protein 3 (RBM3): Clues in hypothermia, cancer biology and apoptosis. Protein Pept. Lett., 2016, 23(9), 828-835.
[http://dx.doi.org/10.2174/0929866523666160628090340] [PMID: 27364162]
[51]
Li, S.; Zhang, Z.; Xue, J.; Liu, A.; Zhang, H. Cold-inducible RNA binding protein inhibits H2O2-induced apoptosis in rat cortical neurons. Brain Res., 2012, 1441, 47-52.
[http://dx.doi.org/10.1016/j.brainres.2011.12.053] [PMID: 22297174]
[52]
Liu, J.; Xue, J.; Zhang, H.; Li, S.; Liu, Y.; Xu, D.; Zou, M.; Zhang, Z.; Diao, J. Cloning, expression, and purification of cold inducible RNA-binding protein and its neuroprotective mechanism of action. Brain Res., 2015, 1597, 189-195.
[http://dx.doi.org/10.1016/j.brainres.2014.11.061] [PMID: 25498861]
[53]
Dai, H.; Zhou, Y.; Lu, Y.; Zhang, X.; Zhuang, Z.; Gao, Y.; Liu, G.; Chen, C.; Ma, J.; Li, W.; Hang, C. Decreased expression of CIRP induced by therapeutic hypothermia correlates with reduced early brain injury after subarachnoid hemorrhage. J. Clin. Med., 2022, 11(12), 3411.
[http://dx.doi.org/10.3390/jcm11123411] [PMID: 35743480]
[54]
Liu, A.; Zhang, Z.; Li, A.; Xue, J. Effects of hypothermia and cerebral ischemia on cold-inducible RNA-binding protein mRNA expression in rat brain. Brain Res., 2010, 1347, 104-110.
[http://dx.doi.org/10.1016/j.brainres.2010.05.029] [PMID: 20546708]
[55]
Khan, M.M.; Yang, W.L.; Brenner, M.; Bolognese, A.C.; Wang, P. Cold-inducible RNA-binding protein (CIRP) causes sepsis-associated acute lung injury via induction of endoplasmic reticulum stress. Sci. Rep., 2017, 7(1), 41363.
[http://dx.doi.org/10.1038/srep41363] [PMID: 28128330]
[56]
Yang, H.J.; Ju, F.; Guo, X.X.; Ma, S.P.; Wang, L.; Cheng, B.F.; Zhuang, R.J.; Zhang, B.B.; Shi, X.; Feng, Z.W.; Wang, M. RNA-binding protein RBM3 prevents NO-induced apoptosis in human neuroblastoma cells by modulating p38 signaling and miR-143. Sci. Rep., 2017, 7(1), 41738.
[http://dx.doi.org/10.1038/srep41738] [PMID: 28134320]
[57]
Xia, W.; Su, L.; Jiao, J. Cold-induced protein RBM3 orchestrates neurogenesis via modulating Yap mRNA stability in cold stress. J. Cell Biol., 2018, 217(10), 3464-3479.
[http://dx.doi.org/10.1083/jcb.201801143] [PMID: 30037926]
[58]
Neto, F.T.L.; Bach, P.V.; Najari, B.B.; Li, P.S.; Goldstein, M. Spermatogenesis in humans and its affecting factors. Semin. Cell Dev. Biol., 2016, 59, 10-26.
[http://dx.doi.org/10.1016/j.semcdb.2016.04.009] [PMID: 27143445]
[59]
Vince, S.; Žura Žaja, I.; Samardžija, M.; Majić Balić, I.; Vilić, M.; Đuričić, D.; Valpotić, H.; Marković, F.; Milinković-Tur, S. Age-related differences of semen quality, seminal plasma, and spermatozoa antioxidative and oxidative stress variables in bulls during cold and warm periods of the year. Animal, 2018, 12(3), 559-568.
[http://dx.doi.org/10.1017/S1751731117001811] [PMID: 28735578]
[60]
Masuda, T.; Itoh, K.; Higashitsuji, H.; Higashitsuji, H.; Nakazawa, N.; Sakurai, T.; Liu, Y.; Tokuchi, H.; Fujita, T.; Zhao, Y.; Nishiyama, H.; Tanaka, T.; Fukumoto, M.; Ikawa, M.; Okabe, M.; Fujita, J. Cold-inducible RNA-binding protein (CIRP) interacts with Dyrk1b/Mirk and promotes proliferation of immature male germ cells in mice. Proc. Natl. Acad. Sci. USA, 2012, 109(27), 10885-10890.
[http://dx.doi.org/10.1073/pnas.1121524109] [PMID: 22711815]
[61]
Hsu, H.K.; Shao, P.L.; Tsai, K.L.; Shih, H.C.; Lee, T.Y.; Hsu, C. Gene regulation by NMDA receptor activation in the SDN-POA neurons of male rats during sexual development. J. Mol. Endocrinol., 2005, 34(2), 433-445.
[http://dx.doi.org/10.1677/jme.1.01601] [PMID: 15821108]
[62]
Banks, S.; King, S.A.; Irvine, D.S.; Saunders, P.T.K. Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reproduction, 2005, 129(4), 505-514.
[http://dx.doi.org/10.1530/rep.1.00531] [PMID: 15798026]
[63]
Pan, Y.; Cui, Y.; He, H.; Baloch, A.R.; Fan, J.; Xu, G.; He, J.; Yang, K.; Li, G.; Yu, S. Developmental competence of mature yak vitrified–warmed oocytes is enhanced by IGF-I via modulation of CIRP during in vitro maturation. Cryobiology, 2015, 71(3), 493-498.
[http://dx.doi.org/10.1016/j.cryobiol.2015.10.150] [PMID: 26519204]
[64]
Jo, J.W.; Jee, B.C.; Lee, J.R.; Suh, C.S. Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence. Fertil. Steril., 2011, 96(5), 1239-1245.
[http://dx.doi.org/10.1016/j.fertnstert.2011.08.023] [PMID: 21917250]
[65]
Rodprasert, W.; Virtanen, H.E.; Mäkelä, J.A.; Toppari, J. Hypogonadism and cryptorchidism. Front. Endocrinol. (Lausanne), 2020, 10, 906.
[http://dx.doi.org/10.3389/fendo.2019.00906] [PMID: 32010061]
[66]
Lee, P.A.; Houk, C.P. Cryptorchidism. Curr. Opin. Endocrinol. Diabetes Obes., 2013, 20(3), 210-216.
[http://dx.doi.org/10.1097/MED.0b013e32835ffc7d] [PMID: 23493040]
[67]
Griveau, J.F.; Lannou, D.L. Reactive oxygen species and human spermatozoa: physiology and pathology. Int. J. Androl., 1997, 20(2), 61-69.
[http://dx.doi.org/10.1046/j.1365-2605.1997.00044.x] [PMID: 9292315]
[68]
Durairajanayagam, D.; Agarwal, A.; Ong, C. Causes, effects and molecular mechanisms of testicular heat stress. Reprod. Biomed. Online, 2015, 30(1), 14-27.
[http://dx.doi.org/10.1016/j.rbmo.2014.09.018] [PMID: 25456164]
[69]
Agarwal, A.; Hamada, A.; Esteves, S.C. Insight into oxidative stress in varicocele-associated male infertility: Part 1. Nat. Rev. Urol., 2012, 9(12), 678-690.
[http://dx.doi.org/10.1038/nrurol.2012.197] [PMID: 23165403]
[70]
Zhou, K.W.; Zheng, X.M.; Yang, Z.W.; Zhang, L.; Chen, H.D. Overexpression of CIRP may reduce testicular damage induced by cryptorchidism. Clin. Invest. Med., 2009, 32(2), 103.
[http://dx.doi.org/10.25011/cim.v32i2.6027] [PMID: 19331798]
[71]
Lee, H.N.; Ahn, S.M.; Jang, H.H. Cold-inducible RNA-binding protein, CIRP, inhibits DNA damage-induced apoptosis by regulating p53. Biochem. Biophys. Res. Commun., 2015, 464(3), 916-921.
[http://dx.doi.org/10.1016/j.bbrc.2015.07.066] [PMID: 26188505]
[72]
Xia, Z.P.; Zheng, X.M.; Zheng, H.; Liu, X.J.; Liu, G.Y.; Wang, X.H. Downregulation of cold-inducible RNA-binding protein activates mitogen-activated protein kinases and impairs spermatogenic function in mouse testes. Asian J. Androl., 2012, 14(6), 884-889.
[http://dx.doi.org/10.1038/aja.2012.71] [PMID: 23001445]
[73]
Ferry, A.L.; Vanderklish, P.W.; Dupont-Versteegden, E.E. Enhanced survival of skeletal muscle myoblasts in response to overexpression of cold shock protein RBM3. Am. J. Physiol. Cell Physiol., 2011, 301(2), C392-C402.
[http://dx.doi.org/10.1152/ajpcell.00098.2011] [PMID: 21593448]
[74]
Wang, Z.Q.; Watanabe, Y.; Toki, A.; Itano, T. Altered distribution of Sertoli cell vimentin and increased apoptosis in cryptorchid rats. J. Pediatr. Surg., 2002, 37(4), 648-652.
[http://dx.doi.org/10.1053/jpsu.2002.31630] [PMID: 11912528]
[75]
Ferragut Cardoso, A.P.; Gomide, L.M.M.; Souza, N.P.; de Jesus, C.M.N.; Arnold, L.L.; Cohen, S.M.; de Camargo, J.L.V.; Nascimento e Pontes, M.G. Time response of rat testicular alterations induced by cryptorchidism and orchiopexy. Int. J. Exp. Pathol., 2021, 102(1), 57-69.
[http://dx.doi.org/10.1111/iep.12384] [PMID: 33502821]
[76]
Dündar, M.; Koçak, I.; Çulhaci, N.; Erol, H. Determination of apoptosis through Bax expression in cryptorchid testis: An experimental study. Pathol. Oncol. Res., 2005, 11(3), 170-173.
[http://dx.doi.org/10.1007/BF02893394] [PMID: 16195771]
[77]
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]
[78]
He, H.; Altomare, D.; Ozer, U.; Xu, H.; Creek, K.; Chen, H.; Xu, P. Cancer cell-selective killing polymer/copper combination. Biomater. Sci., 2016, 4(1), 115-120.
[http://dx.doi.org/10.1039/C5BM00325C] [PMID: 26568413]
[79]
Salomonsson, A.; Micke, P.; Mattsson, J.S.M.; La Fleur, L.; Isaksson, J.; Jönsson, M.; Nodin, B.; Botling, J.; Uhlén, M.; Jirström, K.; Staaf, J.; Planck, M.; Brunnström, H. Comprehensive analysis of RNA binding motif protein 3 (RBM3) in non‐small cell lung cancer. Cancer Med., 2020, 9(15), 5609-5619.
[http://dx.doi.org/10.1002/cam4.3149] [PMID: 32491279]
[80]
Carleton, N.M.; Zhu, G.; Miller, M.C.; Davis, C.; Kulkarni, P.; Veltri, R.W. Characterization of RNA‐binding motif 3 (RBM3) protein levels and nuclear architecture changes in aggressive and recurrent prostate cancer. Cancer Rep., 2020, 3(3), e1237.
[http://dx.doi.org/10.1002/cnr2.1237] [PMID: 32587951]
[81]
Mangé, A.; Lacombe, J.; Bascoul-Mollevi, C.; Jarlier, M.; Lamy, P.J.; Rouanet, P.; Maudelonde, T.; Solassol, J. Serum autoantibody signature of ductal carcinoma in situ progression to invasive breast cancer. Clin. Cancer Res., 2012, 18(7), 1992-2000.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-2527] [PMID: 22322670]
[82]
Wu, Y.; Guo, X.; Brandt, Y.; Hathaway, H.J.; Hartley, R.S. Three-dimensional collagen represses cyclin E1 via β1 integrin in invasive breast cancer cells. Breast Cancer Res. Treat., 2011, 127(2), 397-406.
[http://dx.doi.org/10.1007/s10549-010-1013-x] [PMID: 20607601]
[83]
Guo, X.; Wu, Y.; Hartley, R.S. Cold-inducible RNA-binding protein contributes to human antigen R and cyclin E1 deregulation in breast cancer. Mol. Carcinog., 2010, 49(2), 130-140.
[http://dx.doi.org/10.1002/mc.20582] [PMID: 19777567]
[84]
Milioli, H.H.; Alexandrou, S.; Lim, E.; Caldon, C.E. Cyclin E1 and cyclin E2 in ER+ breast cancer: Prospects as biomarkers and therapeutic targets. Endocr. Relat. Cancer, 2020, 27(5), R93-R112.
[http://dx.doi.org/10.1530/ERC-19-0501] [PMID: 32061162]
[85]
Hamid, A.A.; Mandai, M.; Fujita, J.; Nanbu, K.; Kariya, M.; Kusakari, T.; Fukuhara, K.; Fujii, S. Expression of cold-inducible RNA-binding protein in the normal endometrium, endometrial hyperplasia, and endometrial carcinoma. Int. J. Gynecol. Pathol., 2003, 22(3), 240-247.
[http://dx.doi.org/10.1097/01.PGP.0000070851.25718.EC] [PMID: 12819390]
[86]
Sun, A.; Zhang, H.; Heng, X.; Pang, Q.; Sun, A. Expression of cold-inducible RNA-binding protein (CIRP) in pituitary adenoma and its relationships with tumor recurrence. Med. Sci. Monit., 2015, 21, 1256-1260.
[http://dx.doi.org/10.12659/MSM.893128] [PMID: 25934796]
[87]
Ehlén, Å.; Brennan, D.J.; Nodin, B.; O’Connor, D.P.; Eberhard, J.; Alvarado-Kristensson, M.; Jeffrey, I.B.; Manjer, J.; Brändstedt, J.; Uhlén, M.; Pontén, F.; Jirström, K. Expression of the RNA-binding protein RBM3 is associated with a favourable prognosis and cisplatin sensitivity in epithelial ovarian cancer. J. Transl. Med., 2010, 8(1), 78.
[http://dx.doi.org/10.1186/1479-5876-8-78] [PMID: 20727170]
[88]
Ehlén, Õ.; Nodin, B.; Rexhepaj, E.; Brändstedt, J.; Uhlén, M.; Alvarado-Kristensson, M.; Pontén, F.; Brennan, D.J.; Jirström, K. RBM3-regulated genes promote DNA integrity and affect clinical outcome in epithelial ovarian cancer. Transl. Oncol., 2011, 4(4), 212-IN1.
[http://dx.doi.org/10.1593/tlo.11106] [PMID: 21804916]
[89]
Zhou, R.B.; Lu, X.L.; Zhang, C.Y.; Yin, D.C. RNA binding motif protein 3: a potential biomarker in cancer and therapeutic target in neuroprotection. Oncotarget, 2017, 8(13), 22235-22250.
[http://dx.doi.org/10.18632/oncotarget.14755] [PMID: 28118608]
[90]
Grupp, K.; Wilking, J.; Prien, K.; Hube-Magg, C.; Sirma, H.; Simon, R.; Steurer, S.; Budäus, L.; Haese, A.; Izbicki, J.; Sauter, G.; Minner, S.; Schlomm, T.; Tsourlakis, M.C. High RNA-binding motif protein 3 expression is an independent prognostic marker in operated prostate cancer and tightly linked to ERG activation and PTEN deletions. Eur. J. Cancer, 2014, 50(4), 852-861.
[http://dx.doi.org/10.1016/j.ejca.2013.12.003] [PMID: 24380696]
[91]
Jonsson, L.; Gaber, A.; Ulmert, D.; Uhlén, M.; Bjartell, A.; Jirström, K. High RBM3 expression in prostate cancer independently predicts a reduced risk of biochemical recurrence and disease progression. Diagn. Pathol., 2011, 6(1), 91.
[http://dx.doi.org/10.1186/1746-1596-6-91] [PMID: 21955582]
[92]
Zeng, Y.; Wodzenski, D.; Gao, D.; Shiraishi, T.; Terada, N.; Li, Y.; Vander Griend, D.J.; Luo, J.; Kong, C.; Getzenberg, R.H.; Kulkarni, P. Stress-response protein RBM3 attenuates the stem-like properties of prostate cancer cells by interfering with CD44 variant splicing. Cancer Res., 2013, 73(13), 4123-4133.
[http://dx.doi.org/10.1158/0008-5472.CAN-12-1343] [PMID: 23667174]
[93]
Hanahan, D.; Weinberg, R.A. The hallmarks of cancer. Cell, 2000, 100(1), 57-70.
[http://dx.doi.org/10.1016/S0092-8674(00)81683-9] [PMID: 10647931]
[94]
Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell, 2011, 144(5), 646-674.
[http://dx.doi.org/10.1016/j.cell.2011.02.013] [PMID: 21376230]
[95]
Adamo, P.; Ladomery, M.R. The oncogene ERG: a key factor in prostate cancer. Oncogene, 2016, 35(4), 403-414.
[http://dx.doi.org/10.1038/onc.2015.109] [PMID: 25915839]
[96]
Keniry, M.; Parsons, R. The role of PTEN signaling perturbations in cancer and in targeted therapy. Oncogene, 2008, 27(41), 5477-5485.
[http://dx.doi.org/10.1038/onc.2008.248] [PMID: 18794882]
[97]
Martínez-Arribas, F.; Agudo, D.; Pollán, M.; Gómez-Esquer, F.; Díaz-Gil, G.; Lucas, R.; Schneider, J. Positive correlation between the expression of X-chromosomeRBM genes (RBMX, RBM3, RBM10) and the proapoptoticBax gene in human breast cancer. J. Cell. Biochem., 2006, 97(6), 1275-1282.
[http://dx.doi.org/10.1002/jcb.20725] [PMID: 16552754]
[98]
Jögi, A.; Brennan, D.J.; Rydén, L.; Magnusson, K.; Fernö, M.; Stål, O.; Borgquist, S.; Uhlen, M.; Landberg, G.; Påhlman, S.; Pontén, F.; Jirström, K. Nuclear expression of the RNA-binding protein RBM3 is associated with an improved clinical outcome in breast cancer. Mod. Pathol., 2009, 22(12), 1564-1574.
[http://dx.doi.org/10.1038/modpathol.2009.124] [PMID: 19734850]
[99]
Olofsson, S.E.; Nodin, B.; Gaber, A.; Eberhard, J.; Uhlén, M.; Jirström, K.; Jerkeman, M. Low RBM3 protein expression correlates with clinical stage, prognostic classification and increased risk of treatment failure in testicular non-seminomatous germ cell cancer. PLoS One, 2015, 10(3), e0121300.
[http://dx.doi.org/10.1371/journal.pone.0121300] [PMID: 25811459]
[100]
Boman, K.; Segersten, U.; Ahlgren, G.; Eberhard, J.; Uhlén, M.; Jirström, K.; Malmström, P.U. Decreased expression of RNA-binding motif protein 3 correlates with tumour progression and poor prognosis in urothelial bladder cancer. BMC Urol., 2013, 13(1), 17.
[http://dx.doi.org/10.1186/1471-2490-13-17] [PMID: 23565664]
[101]
Ye, F.; Jin, P.; Cai, X.; Cai, P.; Cai, H. High RNA-binding motif protein 3 (RBM3) expression is independently associated with prolonged overall survival in intestinal-type gastric cancer. Med. Sci. Monit., 2017, 23, 6033-6041.
[http://dx.doi.org/10.12659/MSM.905314] [PMID: 29263314]
[102]
Gao, G.; Shi, X.; Long, Y.; Yao, Z.; Shen, J.; Shen, L. The prognostic and clinicopathological significance of RBM3 in the survival of patients with tumor. Medicine, 2020, 99(19), e20002.
[http://dx.doi.org/10.1097/MD.0000000000020002] [PMID: 32384455]
[103]
Jonsson, L.; Bergman, J.; Nodin, B.; Manjer, J.; Pontén, F.; Uhlén, M.; Jirström, K. Low RBM3 protein expression correlates with tumour progression and poor prognosis in malignant melanoma: An analysis of 215 cases from the Malmö Diet and Cancer Study. J. Transl. Med., 2011, 9(1), 114.
[http://dx.doi.org/10.1186/1479-5876-9-114] [PMID: 21777469]
[104]
Zhang, H.T.; Zhang, Z.W.; Xue, J.H.; Kong, H.B.; Liu, A.J.; Li, S.C.; Liu, Y.X.; Xu, D.G. Differential expression of the RNA-binding motif protein 3 in human astrocytoma. Chin. Med. J. (Engl.), 2013, 126(10), 1948-1952.
[PMID: 23673116]

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