96 남윤권ㆍ이상윤ㆍ김은정,,, (Fernandes et al., 8; Ahi et al., 13).. (Acipenser species) (Actinopterygii) (Birstein et al., 1997). (Teleostei) (holoblastic cleav
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1 한수지 51(1), 95-16, 18 Note Korean J Fish Aquat Sci 51(1),95-16,18 러시아철갑상어 (Acipenser gueldenstaedtii) 발생시료의 RT-qPCR 분석을위한내재대조군유전자의선정 남윤권 * 이상윤 김은정 부경대학교해양바이오신소재학과 Evaluation of Candidate Housekeeping Genes for the Normalization of RT-qPCR Analysis using Developing Embryos and Prolarvae in Russian Sturgeon Acipenser gueldenstaedtii Yoon Kwon Nam*, Sang Yoon Lee and Eun Jeong Kim Department of Marine Bio-Materials and Aquaculture, Pukyong National University, Busan 48513, Korea To evaluate appropriate reference genes for the normalization of quantitative reverse transcription PCR (RT-qPCR) data with embryonic and larval samples from Russian sturgeon Acipenser gueldenstaedtii, the expression stability of eight candidate housekeeping genes, including beta-actin (ACTB), elongation factor-1a (EF1A), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), histone 2A (H2A), ribosomal protein L5 (RPL5), ribosomal protein L7 (RPL7), succinate dehydrogenase (SDHA), and ubiquitin-conjugating enzyme E2 (UBE2A), were tested using embryonic samples from 12 developmental stages and larval samples from 11 ontogenic stages. Based on the stability rankings from three statistic software packages, genorm, NormFinder, and BestKeeper, the expression stability of the embryonic subset was ranked as UBE2A>H2A>SDHA>GAPDH>RPL5>EF1A>ACTB>RPL7. On the other hand, the ranking in the larval subset was determined as UBE2A>GAPDH>SDHA>RPL5>RPL7>H2A>EF1A>AC TB. When the two subsets were combined, the overall ranking was UBE2A>SDHA>H2A>RPL5>GAPDH>EF1A> ACTB>RPL7. Taken together, our data suggest that UBE2A and SDHA are recommended as suitable references for developmental and ontogenic samples of this sturgeon species, whereas traditional housekeepers such as ACTB and GAPDH may not be suitable candidates. Key words: Russian sturgeon, Acipenser gueldenstaedtii, RT-qPCR assay, normalization control, reference genes 서론 PCR (quantitative reverse transcription-pcr; RT-qPCR),. RNA (template) (reference gene) (normalization) (Udvardi et al., 8)., (housekeeping gene) (Bustin et al., 9).,, RTqPCR (Taylor et al., 13; Yuan et al., 14; Lee and Nam, 16)., (Jaramillo et al., 17). Korean J Fish Aquat Sci 51(1) 95-16, February 18 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial Licens ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Received 5 January 18; Revised 24 January 18; Accepted 25 January 18 *Corresponding author: Tel: Fax: address: yoonknam@pknu.ac.kr Copyright 18 The Korean Society of Fisheries and Aquatic Science 95 pissn: , eissn:
2 96 남윤권ㆍ이상윤ㆍ김은정,,, (Fernandes et al., 8; Ahi et al., 13).. (Acipenser species) (Actinopterygii) (Birstein et al., 1997). (Teleostei) (holoblastic cleavage), ( ), (blastomeres). (pronephros) (Bolker, 1993; Cooper and Virta, 7; Park et al., 13a).,, (swimming behavior), (rheotaxis), (phototaxis) (Gisbert and Williot, 1997; Gisbert and Ruban, 3; Park et al., 13b).,. (Acipenser gueldenstaedtii), RT-qPCR. 재료및방법 실험어류, 인공수정및발생시료확보 2. luteinizing hormone-releasing hormone analog (LHRH-a; Sigma-Aldrich, St. Louis, MO, USA) 8 g/kg, g/kg, ( 24-3 ), 24 3 (Park and Chapman, 5) 1:1. 1, 1:1 mating. Fuller s earth (Dettlaff et al., 1993), 12. ( h post fertilization; HPF), 1 (2.2 HPF), 5-6 (7.5 HPF), (9.2 HPF), ( HPF), 7% (28.5 HPF), (33.5 HPF), (4 HPF), (56 HPF), (73.5 HPF), (95 HPF), (1 HPF) , (-8 )., (19 ) (1 m 2 m.3 m; W D H) ( 8 ) (Artemia nauplii) 11 (1 day post hatching; 1 DPH 11 DPH ) 후보유전자및프라이머디자인 1 next generation sequencing (NGS) ( transcriptome ). 1, 8. 8 beta-cytoskeletal actin (ACTB), elongation factor-1 alpha (EF1A), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), histone 2A (H2A), ribosomal protein L5 (RPL5), ribosomal protein L7 (RPL7), succinate dehydrogenase (SDHA) ubiquitin conjugating enzyme E2 (UBE2A), RT-qPCR primer
3 러시아철갑상어발생시료의 RT-qPCR 분석용내재대조군유전자 97 RT-PCR RT-PCR. ( mers), G+C content (45-6%), melting temperature (55-65 ) (15- bp) 2-3 primer PCR (PCR efficiency; E). PCR (E) cdna Light Cycler 48 realtime PCR system, 94% PCR. PCR 1.5% (agarose gel) (ethidium-bromide; Et-Br). Table 1. RNA 분리, cdna 합성및 RT-qPCR 분석 TriPure Reagent (Roche Applied Science) 1 total RNA RNeasy Plus Mini Kit (Qiagen Hilden, Germany), DNA RNase-Free DNase. total RNA MOPS-formaldehyde gel 28S rrna 18S rrna. Total RNA Libar S7 (Biochrom Ltd., UK) (26 nm/28 nm 26 nm/23 nm) Total RNA cdna RNA 2 g oligo-d(t) primer ( mers; Bioneer, Korea) random primer (random nonamers; Takara Bio Inc., Japan) (reverse transcription), omniscript RT kit (Qiagen). nanodrop 1 (Thermo Fisher Scientific, USA), DNase free water 4, cdna 2 L qpcr. PCR light cycler 48 System (Roche Applied Science) SYBR green I master (roche applied science) 95, , melting curve. cdna 3. 유전자발현안정성평가 2 33 ( ) Table 1. Summarized information on the housekeeping gene candidates and qpcr assay primers used in the present study Gene Description Accession no. Primers (5 -to-3 ) Amplicon size (bp) PCR efficiency (%) ACTB Beta-cytoskeletal actin KR EF1A Elongation factor-1 alpha KR GAPDH Glyceraldehyde 3-phosphate dehydrogenase MG H2A Histone 2A KP RPL5 Ribosomal protein L5 MG72283 RPL7 Ribosomal protein L7 MG SDHA Succinate dehydrogenase MG UBE2A Ubiquitin conjugating enzyme E2 MG TCCCTGGAGAAGAGCTATGA ACAGGTCCTTACGGATGTCA ACAACATGCTGGAGACCAGT CGATACCGCCAATCTTGTAG GGCTAAGCGTGTCATCATCT GTCATGAGACCCTCAACGAT CTCGTGCTAAGGCAAAGACT CAGGATTTCAGCAGTCAGGT AAGGAGTTCAACGCAGAGGT ATAGCAGCATGAGCCTTGGT TCAGACTTCGCCAGATCTTC CAGAGGAATACGCTGCTTGT GGAGTTTGTGCAGTTCCATC ACAACATCTCGAGAGGCAAG CTCTTCCTCGCATCATAAGG CCCAGGTATGGTACATTTGC
4 98 남윤권ㆍ이상윤ㆍ김은정 3 (biological replication) 198 cdna (template), cdna 3 qpcr (technical replication) 594 quantification cycle (raw Cq data). cdna (technical replication) (median Cq),. genorm, NormFinder BestKeeper., genorm stability value (M; cutoff=1.5) pairwise (V; cutoff=.15), M (Hellemans et al., 7). NormFinder PCR efficiency Cq (relative quantity) (Andersen et al., 4), BestKeeper coefficient of determination Cq (geometric mean) P (Pfaffl et al., 4). (embryonic subset), (larval subset). 결과 qpcr 의 Cq 데이터패턴 PCR % PCR (Schmittgen and Livak, 8; Doak and Zaïr, 12), melting curve (data not shown). (embryonic subset) 8 Cq, ACTB.1 (mean) Cq ( =.34), 7 EF1A 39.7 Cq ( =39.35). H2A RPL7 4 (GAPDH, RPL5, SDHA UBE2A). Cq, H2A Cq, UBE2 SDHA. EF1A Cq (Fig. 1). (larval subset) Cq, Cq value Cq value Cq value Embryonic subset ACTB EF1A GAPDH H2A RPL5 RPL7 SDHA UBE2A Larval subset ACTB EF1A GAPDH H2A RPL5 RPL7 SDHA UBE2A Total ACTB EF1A GAPDH H2A RPL5 RPL7 SDHA UBE2A Fig. 1. Expression profiles (Cq values) of eight housekeeping gene candidates in embryonic and larval subsets, and also in combined set. In the box plot, the lower and upper boundaries of each box indicate the 25 th and 75 th percentiles, respectively. Whiskers above and below the box are the 9 th and 1 th percentiles, respectively. A black line within the box indicates the median value. The red line indicated by arrow head within the box is the mean value. ACTB, beta-cytoskeletal actin; EF1A, elongation factor-1 alpha; GAPDH, glyceraldehyde 3-phosphate dehydrogenase; H2A, histone 2A; RPL5, ribosomal protein L5; RPL7, ribosomal protein L7SDHA, succinate dehydrogenase; SDHA, succinate dehydrogenase; UBE2A, Ubiquitin conjugating enzyme E2.
5 러시아철갑상어발생시료의 RT-qPCR 분석용내재대조군유전자 99 (Cq ). Cq ( Cq ) GAPDH, RPL7 ACTB, H2A Cq. ACTB ( =16.3) RPL7 ( =16.4), GAPDH ( =18.51) EF1A ( =35.56). Cq, ACTB, EF1A, GAPDH RPL7, H2A (Fig. 1). (subsets) Cq, 8 ACTB RPL7, EF1A., GAPDH Cq RPL7, EF1A, ACTB, RPL5, H2A (Fig. 1). 발생배에서의유전자발현안정성평가 3, 3. genorm SDHA UBE2A, ACTB RPL7. NormFinder GAPDH RPL5 1 2 genorm ACTB RPL Best- Keeper H2A UBE2, RPL7 EF1A. 3, UBE2A (geomean of ranking value; GRV 2.) H2A (GRV=2.29), ACTB (GRV=6.84) RPL7 (GRV=7.). GRV 8 UBE2>H2A >SDHA>GAPDH>RPL5>EF1A>ACTB>RPL7 (Fig. 2). 자어발달과정에서의유전자발현안정성평가 11, genorm NormFinder,, BestKeeper. genorm SDHA UBE2A M ( ) RPL7 ACTB. genorm SDHA/UBE2A>EF1A>H2A>RPL5>GAPDH>RPL7 >ACTB. NormFinder RPL5>GAPDH>H2A>SD HA>UBE2>EF1A>RPL7>ACTB, 1 2, 4 5. BestKeeper RPL7 GAPDH, 7 4. H2A 5. BestKeeper RPL7> GAPDH>UBE2A>ACTB>H2A>SDHA>EF1A>RPL5. GRV UBE2A (GRV=2.47)>GAPDH>S DHA>RPL5>RPL7>H2A>EF1A>ACTB (GRV=6.35) (Fig. 3). 전체시료 ( 발생배및자어발달 ) 에서의유전자발현안정성평가 11. genorm, SDHA/UBE2A, ACTB RPL7 (SDHA/UBE2A>EF1A>H2A>RPL5>GAPDH>RPL7>A CTB). NormFinder GAPDH RPL5, genorm RPL7 ACTB (GAPDH>RPL5>SDHA>U BE2A>H2A>EF1A>RPL7>ACTB). BestKeeper H2A 2 3 UBE2A
6 1 남윤권ㆍ이상윤ㆍ김은정 genorm 25 NormFinder Stability value (M) Stability value SDHA UBE2A EF1A H2A RPL5 GAPDH RPL7 ACTB GAPDH RPL5 H2A UBE2A SDHA EF1A RPL7 ACTB Most stable Least stable Most stable Least stable SD [±Cq] BestKeeper Geomean of ranking value H2A UBE2A SDHA GAPDH ACTB RPL5 RPL7 EF1A. UBE2A H2A SDHA GAPDH RPL5 EF1A ACTB RPL7 Most stable Least stable Most stable Least stable Fig. 2. Expression stability rankings of eight housekeeping genes in embryonic subset as addressed by genorm, NormFinder and Best- Keeper programs. The overall ranking of each gene based on the geomean of ranking values from the three software programs are also provided. ACTB, beta-cytoskeletal actin; EF1A, elongation factor-1 alpha; GAPDH, glyceraldehyde 3-phosphate dehydrogenase; H2A, histone 2A; RPL5, ribosomal protein L5; RPL7, ribosomal protein L7SDHA, succinate dehydrogenase; SDHA, succinate dehydrogenase; UBE2A, Ubiquitin conjugating enzyme E2. (H2A>UBE2A>SDHA>RPL5>ACTB>EF1 A>RPL7>GAPDH). GRV UBE2A (GRV=2.)>SDHA (2.8)>H2A (2.71)>RPL5 (3.42)>GAPDH (3.63)>EF1A (4.76)>ACTB (6.84)>RPL7 (7.) UBE2A SDHA, ACTB RPL7 (Fig. 4). 고찰 8 (ACTB), (EF1A), (GAPDH), (chromatin) (H2A), (RPL5 RPL7), (SDHA), (UBE2A) Cq,. Cq (Cq ). GAPDH, RPL7 EF1A, (Dettlaff et al., 1993; Park et al., 13b). ACTB (organ differentiation) (larval
7 러시아철갑상어발생시료의 RT-qPCR 분석용내재대조군유전자 Stability value (M) genorm Stability value NormFinder SDHA UBE2A EF1A H2A RPL5 GAPDH RPL7 ACTB RPL5 GAPDH H2A SDHA UBE2A EF1A RPL7 ACTB Most stable Least stable Most stable Least stable SD [±Cq] BestKeeper Geomean of ranking value RPL7 GAPDHUBE2A ACTB H2A SDHA EF1A RPL5. UBE2A GAPDH SDHA RPL5 RPL7 H2A EF1A ACTB Most stable Least stable Most stable Least stable Fig. 3. Expression stability rankings of eight housekeeping genes in larval subset as addressed by genorm, NormFinder and BestKeeper programs. The overall ranking of each gene based on the geomean of ranking values from the three software programs are also provided. ACTB, beta-cytoskeletal actin; EF1A, elongation factor-1 alpha; GAPDH, glyceraldehyde 3-phosphate dehydrogenase; H2A, histone 2A; RPL5, ribosomal protein L5; RPL7, ribosomal protein L7SDHA, succinate dehydrogenase; SDHA, succinate dehydrogenase; UBE2A, Ubiquitin conjugating enzyme E2. morphogenesis) ACTB (Reece et al., 1992; Reisler and Egelman 7)., H2A Cq,. H2A, oligo-dt random 7 random priming cdna, Cq (López and Samuelsson, 8). UBE2A H2A ACTB RPL7, Cq profile. UBE2A H2A ACTB RPL7. Cq ACTB RPL7 (onset of neurulation) ( 8 ), 7-9. (embryonic body) (pronephros), (head), (somite) (S-heart)
8 12 남윤권ㆍ이상윤ㆍ김은정 6 5 genorm 14 1 NormFinder Stability value (M) 4 3 Stability value SDHA UBE2A EF1A H2A RPL5 GAPDH RPL7 ACTB GAPDH RPL5 SDHA UBE2A H2A EF1A RPL7 ACTB Most stable Least stable Most stable Least stable BestKeeper SD [±Cq] Geomean of ranking value H2A UBE2A SDHA RPL5 ACTB EF1A RPL7 GAPDH. UBE2A SDHA H2A RPL5 GAPDH EF1A ACTB RPL7 Most stable Least stable Most stable Least stable Fig. 4. Expression stability rankings of eight housekeeping genes in the combined dataset including both embryonic and larval subsets. Stability ranking of each gene in genorm, NormFinder and BestKeeper programs were used to calculate geomean of ranking values. ACTB, beta-cytoskeletal actin; EF1A, elongation factor-1 alpha; GAPDH, glyceraldehyde 3-phosphate dehydrogenase; H2A, histone 2A; RPL5, ribosomal protein L5; RPL7, ribosomal protein L7SDHA, succinate dehydrogenase; SDHA, succinate dehydrogenase; UBE2A, Ubiquitin conjugating enzyme E2. (Dettlaff et al., 1993; Park et al., 13a),,, ACTB RPL7. EF1A, RPL5, GAPDH, ACTB RPL7., ( ) RT-qPCR,, (glycolysis) UBE2A H2A. GRV, UBE2A. UBE2A GAPDH SDHA (GRV=2.88 ),,, (Park et al., 13b). RPL5, RPL7 H2A GRV ( ), RPL5 RPL7, GRV
9 러시아철갑상어발생시료의 RT-qPCR 분석용내재대조군유전자 13. H2A Cq,. ACTB EF1A ACTB. 4 DPH 5 DPH 8-9 DPH., 4-5 DPH, 8-9 DPH pigment plug (, ) (Dettlaff et al., 1993).. Cq, UBE2A (genorm 1, NormFinder 4 BestKeeper 2 ). UBE2A Arctic charr Salvelinus alpinus (Ahi et al., 13) Atlantic halibut Hippoglossus hippoglossus (zygotic transcription ) (Øvergård et al., 1),. UBE2A SDHA genorm 1, NormFinder 3, BestKeeper 3 UBE2A. GRV 3 H2A, H2A BestKeeper. SDHA H2A,.,, (Souza et al., 13; Luchsinger et al., 14; Yan et al., 14; Omondi et al., 15; Steinhauser et al., 17)., (RPL5/7, EF1A, GAPDH, ACTB), GAPDH,., RT-qPCR ACTB, GAPDH RPL.,. ACTB,., Arctic charr S. alpinus (Ahi et al., 13) Atlantic halibut H. hippoglossus (Fernandes et al., 8) ACTB, European seabass Dicentrarchus labrax (Mitter et al., 9), Senegalese sole Solea senegalensis (Infante et al., 8), Atlantic halibut (Infante et al., 8) ACTB. GAPDH RT-qPCR, GAPDH (Fernandes et al., 8; Infante et al., 8; Mitter et al., 9; García-Fernández et al., 16)., 2 GAPDH paralogs isoform (Cho et al., 8; Kim and Nam, 8; Lee et al., 13), GAPDH isoform, GAPDH paralog isoform (Infante et al., 8). RPL5 RPL7 (Zhang and Hu, 7; Lόpez-Landavery et al. 14; Lee and Nam,
10 14 남윤권ㆍ이상윤ㆍ김은정 16),. Atlantic halibut ribosomal protein S4 (RPS4), ribosomal protein L13 (RPL13), RPL7, RPL7 (Øvergård et al., 1)., RPL7,,., RT-qPCR ACTB, GAPDH RPL, UBE2A SDHA. H2A ( ) GAPDH ( ).. 사사 (16).. References Ahi EP, Guðbrandsson J, Kapralova KH, Franzdóttir SR, Snorrason SS, Maier VH and Jónsson ZO. 13. Validation of reference genes for expression studies during craniofacial development in Arctic charr. PLoS One 8, e doi.org/1.1371/journal.pone Andersen CL, Jensen JL and Ørntoft TF. 4. Normalization of real-time quantitative reverse transcription-pcr data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64, org/1.1158/ can Birstein VJ, Hanner R and DeSalle R Phylogeny of the Acipenseriformes: cytogenetic and molecular approaches. Environ Biol Fishes 48, org/1.123/a: Bolker JA The mechanism of gastrulation in the white sturgeon. J Exp Zool 266, jez Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J and Wittwer CT. 9. The MIQE guidelines: minimum information for publication of quantitative realtime PCR experiments. Clin Chem 55, org/1.1373/clinchem Cho YS, Lee SY, Kim KH and Nam YK. 8. Differential modulations of two glyceraldehyde 3-phosphate dehydrogenase mrnas in response to bacterial and viral challenges in a marine teleost Oplegnathus fasciatus (Perciformes). Fish Shellfish Immunol 25, fsi Cooper MS and Virta VC. 7. Evolution of gastrulation in the rayfinned (Actinopterygian) fishes. J Exp Zool B Mol Dev Evol 38, Dettlaff TA, Ginsburg AS and Schmalhausen OI Sturgeon Fishes- Developmental Biology and Aquaculture. Springer- Verlag, Berlin Heidelberg, Germany, Doak SH and Zair Z. 12. Real-time reverse-transcription polymerase chain reaction: technical considerations for gene expression analysis. In: Genetic toxicology: principles and methods, methods in molecular biology. Parry JM and Parry EM, eds. Springer, New York, U.S.A., org/1.17/ _13. Fernandes JMO, Mommens M, Hagen Ø, Babiak I and Solberg C. 8. Selection of suitable reference genes for realtime PCR studies of Atlantic halibut development. Comp Biochem Physiol B 15, cbpb García-Fernández P, Castellanos-Martínez S, Iglesias J, Otero JJ and Gestal C. 16. Selection of reliable reference genes for RT-qPCR studies in Octopus vulgaris paralarvae during development and immune-stimulation. J Invert Pathol 138, Gisbert E and Ruban GI. 3. Ontogenic behavior of Siberian sturgeon, Acipenser baerii: a synthesis between laboratory tests and field data. Environ Biol Fishes 67, doi.org/1.123/a: Gisbert E and Williot P Larval behaviour and effect of the timing of initial feeding on growth and survival of Siberian sturgeon (Acipenser baerii) larvae under small scale hatchery production. Aquaculture 156, org/1.116/s (97)86-. Hellemans J, Mortier G, De Paepe A, Speleman F and Vandesompele J. 7. qbase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8, R19. doi.org/1.1186/gb r19. Infante C, Matsuoka MP, Asensio E, Cañavate JP, Reith M and Manchado M. 8. Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time
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12 16 남윤권ㆍ이상윤ㆍ김은정 genes for gene expression analysis in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae) using reverse transcription quantitative PCR. PLoS One 9, e Zhang Z and Hu J. 7. Development and validation of endogenous reference genes for expression profiling of medaka (Oryzias latipes) exposed to endocrine disrupting chemicals by quantitative real-time RT-PCR. Toxicol Sci 95,
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