Cited by 12Vanadium and Halogenation ChemistryMolecular Biology Techniques and ApplicationsRNA Research and Splicing

Application of ribonucleoside vanadyl complex (RVC) for developing a multifunctional tissue preservative solution

Open access
Shieh, Tzong-Ming, Chen, Chi-Yuan, Hsueh, Chuen, Yu, Cheng-Chia, Chen, Chin-Chuan, Wang, Tong-Hong·2018·PLOS ONE

Abstract

The quality of biological samples greatly affects the accuracy of scientific results. However, RNA in cryopreserved tissues gradually degrades during storage, leading to errors in the results of subsequent experiments. A suitable sample preservative solution can prolong storage and enhance the research value of samples. Here, we developed a sample preservative solution using the properties of the ribonucleoside vanadyl complex (RVC) and compared its effects on RNA and DNA quality, protein activity, and tissue morphology with the commercially available and widely used RNAlater® Stabilization Solution. The results showed that both the RVC-based preservative solution and RNAlater can effectively delay RNA degradation in tissue samples stored at 4°C or -80°C compared with samples stored without any preservative solution. In contrast to RNAlater, the RVC-based preservative solution did not result in damage to the tissue morphology or a loss of protein activity. Additionally, the RVC-based preservative solution did not affect the RNA and genomic DNA contents of the tissue samples or the results of subsequent experimental analyses. An RVC-based reagent can be used as a multifunctional yet relatively inexpensive tissue preservative solution to provide a comprehensive and cost-effective method for preserving samples for tissue banks.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0194393

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 33

  1. [1]Li M, Reilly C. Assessing the quality of hybridized RNA in Affymetrix GeneChips using linear regression. J Biomol Tech. 2008; 19(2): 122– 8.; PubMed Central PMCID: PMCPMC2361161. 19137095 PMC2361161
  2. [2]Viljoen KS, Blackburn JM. Quality assessment and data handling methods for Affymetrix Gene 1.0 ST arrays with variable RNA integrity. BMC Genomics. 2013; 14: 14 doi: 10.1186/1471-2164-14-14; PubMed Central PMCID: PMCPMC3557148. 23324084 PMC3557148 · DOI
  3. [3]Popova T, Mennerich D, Weith A, Quast K. Effect of RNA quality on transcript intensity levels in microarray analysis of human post-mortem brain tissues. BMC Genomics. 2008; 9: 91 doi: 10.1186/1471-2164-9-91; PubMed Central PMCID: PMCPMC2268927. 18298816 PMC2268927 · DOI
  4. [4]Chen EA, Souaiaia T, Herstein JS, Evgrafov OV, Spitsyna VN, Rebolini DF, et al Effect of RNA integrity on uniquely mapped reads in RNA-Seq. BMC Res Notes. 2014; 7: 753 doi: 10.1186/1756-0500-7-753; PubMed Central PMCID: PMCPMC4213542. 25339126 PMC4213542 · DOI
  5. [5]Reiman M, Laan M, Rull K, Sober S. Effects of RNA integrity on transcript quantification by total RNA sequencing of clinically collected human placental samples. FASEB J. 2017; 31(8): 3298– 308. doi: 10.1096/fj.201601031RR. 28446590 · DOI
  6. [6]Le Page C, Kobel M, de Ladurantaye M, Rahimi K, Madore J, Babinszky S, et al Specimen quality evaluation in Canadian biobanks participating in the COEUR repository. Biopreserv Biobank. 2013; 11(2): 83– 93. doi: 10.1089/bio.2012.0044. 24845429 · DOI
  7. [7]Wang TH, Chen CC, Liang KH, Chen CY, Chuang WY, Ueng SH, et al A Multivariate Evaluation of Factors Affecting the Quality of Freshly Frozen Tissue Specimens. Biopreserv Biobank. 2017; 15(4): 344– 9. doi: 10.1089/bio.2016.0104. 28541714 · DOI
  8. [8]Hostein I, Stock N, Soubeyran I, Marty M, De Mascarel I, Bui M, et al Nucleic acid quality preservation by an alcohol-based fixative: comparison with frozen tumors in a routine pathology setting. Diagnostic molecular pathology: the American journal of surgical pathology, part B. 2011; 20(1): 52– 62. doi: 10.1097/PDM.0b013e3181e71ba5. 21326040 · DOI
  9. [9]Hatzis C, Sun H, Yao H, Hubbard RE, Meric-Bernstam F, Babiera GV, et al Effects of tissue handling on RNA integrity and microarray measurements from resected breast cancers. J Natl Cancer Inst. 2011; 103(24): 1871– 83. doi: 10.1093/jnci/djr438; PubMed Central PMCID: PMCPMC3243675. 22034635 PMC3243675 · DOI
  10. [10]Shabihkhani M, Lucey GM, Wei B, Mareninov S, Lou JJ, Vinters HV, et al The procurement, storage, and quality assurance of frozen blood and tissue biospecimens in pathology, biorepository, and biobank settings. Clinical biochemistry. 2014; 47(4–5): 258– 66. doi: 10.1016/j.clinbiochem.2014.01.002; PubMed Central PMCID: PMCPMC3982909. 24424103 PMC3982909 · DOI
  11. [11]Heumuller-Klug S, Sticht C, Kaiser K, Wink E, Hagl C, Wessel L, et al Degradation of intestinal mRNA: a matter of treatment. World J Gastroenterol. 2015; 21(12): 3499– 508. doi: 10.3748/wjg.v21.i12.3499; PubMed Central PMCID: PMCPMC4375571. 25834314 PMC4375571 · DOI
  12. [12]Wang Y, Zheng H, Chen J, Zhong X, Wang Y, Wang Z, et al The Impact of Different Preservation Conditions and Freezing-Thawing Cycles on Quality of RNA, DNA, and Proteins in Cancer Tissue. Biopreserv Biobank. 2015; 13(5): 335– 47. doi: 10.1089/bio.2015.0029. 26484573 · DOI
  13. [13]Martin NM, Cooke KM, Radford CC, Perley LE, Silasi M, Flannery CA. Time course analysis of RNA quality in placenta preserved by RNAlater or flash freezing. Am J Reprod Immunol. 2017; 77(4). doi: 10.1111/aji.12637; PubMed Central PMCID: PMCPMC5397349. 28138995 PMC5397349 · DOI
  14. [14]Hawley D, Aluri H, Armaos H, Kim G, Kublin C, Zoukhri D. Human postmortem lacrimal and submandibular glands stored in RNAlater are suitable for molecular, biochemical, and cell biological studies. Mol Vis. 2016; 22: 1221– 8.; PubMed Central PMCID: PMCPMC5070571. 27777501 PMC5070571
  15. [15]Roos-van Groningen MC, Eikmans M, Baelde HJ, de Heer E, Bruijn JA. Improvement of extraction and processing of RNA from renal biopsies. Kidney Int. 2004; 65(1): 97– 105. doi: 10.1111/j.1523-1755.2004.00366.x. 14675040 · DOI
  16. [16]Viertler C, Groelz D, Gundisch S, Kashofer K, Reischauer B, Riegman PH, et al A new technology for stabilization of biomolecules in tissues for combined histological and molecular analyses. J Mol Diagn. 2012; 14(5): 458– 66. doi: 10.1016/j.jmoldx.2012.05.002. 22749745 · DOI
  17. [17]Berger SL. Isolation of cytoplasmic RNA: ribonucleoside-vanadyl complexes. Methods in enzymology. 1987; 152: 227– 34.. 2443795
  18. [18]Liakh LA, Khil'ko SN, Aspetov RD, Nosik DN, Novokhatskii AS. [ Purification and identification of mRNA of immune (gamma) interferon from human splenocytes]. Biokhimiia. 1983; 48(10): 1739– 46.. 6416307
  19. [19]Berger SL, Birkenmeier CS. Inhibition of intractable nucleases with ribonucleoside—vanadyl complexes: isolation of messenger ribonucleic acid from resting lymphocytes. Biochemistry. 1979; 18(23): 5143– 9.. 497174
  20. [20]del Prete MJ, Vernal R, Dolznig H, Mullner EW, Garcia-Sanz JA. Isolation of polysome-bound mRNA from solid tissues amenable for RT-PCR and profiling experiments. Rna. 2007; 13(3): 414– 21. doi: 10.1261/rna.79407; PubMed Central PMCID: PMCPMC1800518. 17237355 PMC1800518 · DOI
  21. [21]Nicolaides NC, Stoeckert CJ Jr. A simple, efficient method for the separate isolation of RNA and DNA from the same cells. Biotechniques. 1990; 8(2): 154– 6.. 1690560
  22. [22]Frazier AD, Champney WS. The vanadyl ribonucleoside complex inhibits ribosomal subunit formation in Staphylococcus aureus. The Journal of antimicrobial chemotherapy. 2012; 67(9): 2152– 7. doi: 10.1093/jac/dks182; PubMed Central PMCID: PMCPMC3417690. 22643191 PMC3417690 · DOI
  23. [23]Frazier AD, Champney WS. Inhibition of ribosomal subunit synthesis in Escherichia coli by the vanadyl ribonucleoside complex. Curr Microbiol. 2013; 67(2): 226– 33. doi: 10.1007/s00284-013-0350-5; PubMed Central PMCID: PMCPMC3696395. 23512123 PMC3696395 · DOI
  24. [24]Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012; 7(3): 562– 78. doi: 10.1038/nprot.2012.016; PubMed Central PMCID: PMCPMC3334321. 22383036 PMC3334321 · DOI
  25. [25]Smith JJ, Gunasekera TS, Barardi CR, Veal D, Vesey G. Determination of Cryptosporidium parvum oocyst viability by fluorescence in situ hybridization using a ribosomal RNA-directed probe. J Appl Microbiol. 2004; 96(2): 409– 17.. 14723702
  26. [26]Reddy KJ, Gilman M. Preparation of bacterial RNA. Curr Protoc Mol Biol. 2001;Chapter 4:Unit4 doi: 10.1002/0471142727.mb0404s21. 18265238 · DOI
  27. [27]Lee CH, Leeds P, Ross J. Purification and characterization of a polysome-associated endoribonuclease that degrades c-myc mRNA in vitro. The Journal of biological chemistry. 1998; 273(39): 25261– 71.. 9737991
  28. [28]Tregidgo C, Levitt JA, Suhling K. Effect of refractive index on the fluorescence lifetime of green fluorescent protein. Journal of biomedical optics. 2008; 13(3): 031218 doi: 10.1117/1.2937212. 18601542 · DOI
  29. [29]Suhling K, Siegel J, Phillips D, French PM, Leveque-Fort S, Webb SE, et al Imaging the environment of green fluorescent protein. Biophys J. 2002; 83(6): 3589– 95. doi: 10.1016/S0006-3495(02)75359-9; PubMed Central PMCID: PMCPMC1302434. 12496126 PMC1302434 · DOI
  30. [30]Gray JC. The inhibition of ribonuclease activity and the isolation of polysomes from leaves of the french bean, Phaseolus vulgaris. Arch Biochem Biophys. 1974; 163(1): 343– 8.. 4369318
  31. [31]Berger SL, Hitchcock MJ, Zoon KC, Birkenmeier CS, Friedman RM, Chang EH. Characterization of interferon messenger RNA synthesis in Namalva cells. J Biol Chem. 1980; 255(7): 2955– 61.. 7358718
  32. [32]Egberts E, Hackett PB, Traub P. Inhibition of ribonucleases by ribonucleotides and transition state analogs in cell-free extracts from Ehrlich ascites tumor cells. Hoppe Seylers Z Physiol Chem. 1977; 358(4): 475– 90.. 324884
  33. [33]Dickson KA, Haigis MC, Raines RT. Ribonuclease inhibitor: structure and function. Prog Nucleic Acid Res Mol Biol. 2005; 80: 349– 74. doi: 10.1016/S0079-6603(05)80009-1; PubMed Central PMCID: PMCPMC2811166. 16164979 PMC2811166 · DOI

Cited by

Sorted by citations

Authors
Shieh, T.-M., Chen, C.-Y., Hsueh, C., Yu, C.-C., Chen, C.-C., & Wang, T.-H.
Affiliations
  • China Medical University (TW)
  • Chang Gung University of Science and Technology (TW)
  • Chang Gung Memorial Hospital (TW)
  • Chung Shan Medical University (TW)
Corresponding author
Wang, Tong-Hong
Venue
PLOS ONE
Published
2018-03-14
Volume
13
Issue
3
Pages
e0194393
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2793522306
Cited by
12
References
0
Citations by year
2025: 2 · 2024: 3 · 2023: 3 · 2022: 1 · 2020: 3
FWCI
0.27
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Ministry of Science and Technology, Taiwan (MOST 105-2320-B-182A-004-)
  • Chang Gung Medical Foundation (CRRPG3F0071)
Topics
  • Physical Sciences › Chemistry › Inorganic Chemistry › Vanadium and Halogenation Chemistry
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Molecular Biology Techniques and Applications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Keywords
RNA degradation, cryopreservation, tissue banking, RNAlater, DNA integrity, protein activity, tissue morphology, sample preservation
MeSH terms
Animals, Male, Mice, Inbred BALB C, Ribonucleosides, Tissue Preservation, Vanadates, Organ Preservation Solutions, RNA Stability, Mice, Protein Stability

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review