Identification of qRT-PCR reference genes for analysis of opioid gene expression in a hibernator

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 180, Issue 4, 2010, Pages 619-629

  Otis, Jessica P ^a   Ackermann, Laynez W ^b   Denning, Gerene M ^b   Carey, Hannah V ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

Author keywords

Hibernation; Opioids; qRT PCR; Reference genes; Torpor

Indexed keywords

MESSENGER RNA; OPIATE PEPTIDE; PRIMER DNA;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BODY TEMPERATURE; BRAIN; GENE EXPRESSION REGULATION; GENETICS; HEART MUSCLE; HIBERNATION; LIVER; METABOLISM; PHYSIOLOGY; REFERENCE VALUE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCIURIDAE; SEASON; SMALL INTESTINE; UNITED STATES;

ANALYSIS OF VARIANCE; ANIMALS; BODY TEMPERATURE; BRAIN; DNA PRIMERS; GENE EXPRESSION REGULATION; HIBERNATION; INTESTINE, SMALL; LIVER; MYOCARDIUM; OPIOID PEPTIDES; REFERENCE VALUES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SCIURIDAE; SEASONS; WISCONSIN;

ANIMALIA; SCIURIDAE; SPERMOPHILUS;

EID: 77952497876     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-009-0430-9     Document Type: Article

References (56)

1. Andersen CL, Jensen JL, Orntoft TF (2004) 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: 5245-5250.
2. Andrews MT (2007) Advances in molecular biology of hibernation in mammals. Bioessays 29: 431-440.
3. Beckman AL, Llados-Eckman C (1985) Antagonism of brain opioid peptide action reduces hibernation bout duration. Brain Res 325: 201-205.
4. Beckman AL, Dean RR, Wamsley JK (1986) Hippocampal and cortical opioid receptor binding: changes related to the hibernation state. Brain Res 386: 223-231.
5. Blanquicett C, Johnson MR, Heslin M, Diasio RB (2002) Housekeeping gene variability in normal and carcinomatous colorectal and liver tissues: applications in pharmacogenomic gene expression studies. Anal Biochem 303: 209-214.
6. Bourhim N, Kabine M, Elkebbaj MS (1997) Characterization of opioid peptides and opioid receptors in the brain of jerboa (Jaculus orientalis), a hibernating rodent. Brain Res Bull 44: 615-620.
7. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83: 1153-1181.
8. Carey HV, Potter KT, Peters TL, Epperson LE, Rose JC, Martin SL (2006) Hibernating mammals have enhanced survival and reduced gut damage after hemorrhage. FASEB J 20: Abstract #903. 901.
9. Collantes-Fernandez E, Zaballos A, Alvarez-Garcia G, Ortega-Mora LM (2002) Quantitative detection of Neospora caninum in bovine aborted fetuses and experimentally infected mice by real-time PCR. J Clin Microbiol 40: 1194-1198.
10. Crawford FI, Hodgkinson CL, Ivanova E, Logunova LB, Evans GJ, Steinlechner S, Loudon AS (2007) Influence of torpor on cardiac expression of genes involved in the circadian clock and protein turnover in the Siberian hamster (Phodopus sungorus). Physiol Genomics 31: 521-530.
11. Cui Y, Lee TF, Wang LCH (1996) State-dependent changes of brain endogenous opioids in mammalian hibernation. Brain Res Bull 40: 129-133.
12. Cui Y, Lee TF, Westly J, Wang LCH (1997) Autoradiographic determination of changes in opioid receptor binding in the limbic system of the Columbian ground squirrel at different hibernation states. Brain Res 747: 189-194.
13. Dave KR, Prado R, Raval AP, Drew KL, Perez-Pinzon MA (2006) The arctic ground squirrel brain is resistant to injury from cardiac arrest during euthermia. Stroke 37: 1261-1265.
14. de Kok JB, Roelofs RW, Giesendorf BA, Pennings JL, Waas ET, Feuth T, Swinkels DW, Span PN (2005) Normalization of gene expression measurements in tumor tissues: comparison of 13 endogenous control genes. Lab Invest 85: 154-159.
15. Drew KL, Harris MB, LaManna JC, Smith MA, Zhu XW, Ma YL (2004) Hypoxia tolerance in mammalian heterotherms. J Exp Biol 207: 3155-3162.
16. Drew KL, Buck CL, Barnes BM, Christian SL, Rasley BT, Harris MB (2007) Central nervous system regulation of mammalian hibernation: implications for metabolic suppression and ischemia tolerance. J Neurochem 102: 1713-1726.
17. Epperson LE, Martin SL (2002) Quantitative assessment of ground squirrel RNA levels in multiple stages of hibernation. Physiol Genomics 10: 93-102.
18. Ermolinsky B, Pacheco Otalora LF, Arshadmansab MF, Zarei MM, Garrido-Sanabria ER (2008) Differential changes in mGlu2 and mGlu3 gene expression following pilocarpine-induced status epilepticus: a comparative real-time PCR analysis. Brain Res 1226: 173-180.
19. Goidin D, Mamessier A, Staquet MJ, Schmitt D, Berthier-Vergnes O (2001) Ribosomal 18S RNA prevails over glyceraldehyde-3-phosphate dehydrogenase and beta-actin genes as internal standard for quantitative comparison of mRNA levels in invasive and noninvasive human melanoma cell subpopulations. Anal Biochem 295: 17-21.
20. Hansen MC, Nielsen AK, Molin S, Hammer K, Kilstrup M (2001) Changes in rRNA levels during stress invalidates results from mRNA blotting: fluorescence in situ rRNA hybridization permits renormalization for estimation of cellular mRNA levels. J Bacteriol 183: 4747-4751.
21. Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol 141: 317-329.
22. Helgen KM, Cole FR, Helgen LE, Wilson DE (2009) Genetic revision of in the holarctic ground squirrel genus spermophilus. J Mammal 90: 270-305.
23. Hittel D, Storey KB (2001) Differential expression of adipose- and heart-type fatty acid binding proteins in hibernating ground squirrels. Biochim Biophys Acta 1522: 238-243.
24. Hittel D, Storey KB (2002) The translation state of differentially expressed mRNAs in the hibernating thirteen-lined ground squirrel (Spermophilus tridecemlineatus). Arch Biochem Biophys 401: 244-254.
25. Infante C, Matsuoka MP, Asensio E, Canavate JP, Reith M, Manchado M (2008) Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time PCR. BMC Mol Biol 9: 28.
26. Kidd M, Nadler B, Mane S, Eick G, Malfertheiner M, Champaneria M, Pfragner R, Modlin I (2007) GeneChip, geNorm, and gastrointestinal tumors: novel reference genes for real-time PCR. Physiol Genomics 30: 363-370.
27. Kurtz CC, Lindell SL, Mangino MJ, Carey HV (2006) Hibernation confers resistance to intestinal ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 291: 895-901.
28. Langnaese K, John R, Schweizer H, Ebmeyer U, Keilhoff G (2008) Selection of reference genes for quantitative real-time PCR in a rat asphyxial cardiac arrest model. BMC Mol Biol 9: 53.
29. Lindell SL, Klahn SL, Piazza TM, Southard JH, Carey HV (2005) Natural resistance to liver cold ischemia-reperfusion injury associated with the hibernation phenotype. Am J Physiol Gastrointest Liver Physiol 288: G473-G480.
30. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
31. Ma MC, Qian H, Ghassemi F, Zhao P, Xia Y (2005a) Oxygen-sensitive {delta}-opioid receptor-regulated survival and death signals: novel insights into neuronal preconditioning and protection. J Biol Chem 280: 16208-16218.
32. Ma YL, Zhu X, Rivera PM, Toien O, Barnes BM, LaManna JC, Smith MA, Drew KL (2005b) Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 289: R1297-R1306.
33. Margules DL, Goldman B, Finck A (1979) Hibernation: an opioid-dependent state? Brain Res Bull 4: 721-724.
34. Morin P Jr, Ni Z, McMullen DC, Storey KB (2008) Expression of Nrf2 and its downstream gene targets in hibernating 13-lined ground squirrels, Spermophilus tridecemlineatus. Mol Cell Biochem 312: 121-129.
35. Nurnberger F, Lee TF, Jourdan ML, Wang LC (1991) Seasonal changes in methionine-enkephalin immunoreactivity in the brain of a hibernator, Spermophilus columbianus. Brain Res 547: 115-121.
36. Nygard AB, Jorgensen CB, Cirera S, Fredholm M (2007) Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR. BMC Mol Biol 8: 67.
37. O'Hara BF, Watson FL, Srere HK, Kumar H, Wiler SW, Welch SK, Bitting L, Heller HC, Kilduff TS (1999) Gene expression in the brain across the hibernation cycle. J Neurosci 19: 3781-3790.
38. Olsvik PA, Lie KK, Jordal AE, Nilsen TO, Hordvik I (2005) Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon. BMC Mol Biol 6: 21.
39. Peart JN, Gross ER, Gross GJ (2004) Effect of exogenous kappa-opioid receptor activation in rat model of myocardial infarction. J Cardiovasc Pharmacol 43: 410-415.
40. Peirson SN, Butler JN, Foster RG (2003) Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res 31: e73.
41. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26: 509-515.
42. Sigg DC, Coles JA, Gallagher WJ, Oeltgen PR, Iaizzo PA (2001) Opioid preconditioning: myocardial function and energy metabolism. Ann Thorac Surg 72: 1576-1582.
43. Simpson DA, Feeney S, Boyle C, Stitt AW (2000) Retinal VEGF mRNA measured by SYBR green I fluorescence: a versatile approach to quantitative PCR. Mol Vis 6: 178-183.
44. Skovgaard K, Mortensen S, Poulsen KT, Angen O, Heegaard PM (2007) Validation of putative reference genes for qRT-PCR normalization in tissues and blood from pigs infected with Actinobacillus pleuropneumoniae. Vet Immunol Immunopathol 118: 140-146.
45. Soukri A, Valverde F, Hafid N, Elkebbaj MS, Serrano A (1996) Occurrence of a differential expression of the glyceraldehyde-3-phosphate dehydrogenase gene in muscle and liver from euthermic and induced hibernating jerboa (Jaculus orientalis). Gene 181: 139-145.
46. Spinsanti G, Zannolli R, Panti C, Ceccarelli I, Marsili L, Bachiocco V, Frati F, Aloisi AM (2008) Quantitative real-time PCR detection of TRPV1-4 gene expression in human leukocytes from healthy and hyposensitive subjects. Mol Pain 4: 51.
47. Squire TL, Lowe ME, Bauer VW, Andrews MT (2003) Pancreatic triacylglycerol lipase in a hibernating mammal. II. Cold-adapted function and differential expression. Physiol Genomics 16: 131-140.
48. Tamura Y, Shintani M, Nakamura A, Monden M, Shiomi H (2005) Phase-specific central regulatory systems of hibernation in Syrian hamsters. Brain Res 1045: 88-96.
49. van Breukelen F, Martin SL (2002) Invited review: molecular adaptations in mammalian hibernators: unique adaptations or generalized responses? J Appl Physiol 92: 2640-2647.
50. Vandesompele J, De Preter K, Pattyn F, Poppe B, van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
51. Walker JM, Glotzbach SF, Berger RJ, Heller HC (1977) Sleep and hibernation in ground squirrels (Citellus spp): electrophysiological observations. Am J Physiol 233: R213-R221.
52. Yamada H, Chen D, Monstein HJ, Hakanson R (1997) Effects of fasting on the expression of gastrin, cholecystokinin, and somatostatin genes and of various housekeeping genes in the pancreas and upper digestive tract of rats. Biochem Biophys Res Commun 231: 835-838.
53. Yan J, Burman A, Nichols C, Alila L, Showe LC, Showe MK, Boyer BB, Barnes BM, Marr TG (2006) Detection of differential gene expression in brown adipose tissue of hibernating arctic ground squirrels with mouse microarrays. Physiol Genomics 25: 346-353.
54. Yan J, Barnes BM, Kohl F, Marr TG (2008) Modulation of gene expression in hibernating arctic ground squirrels. Physiol Genomics 32: 170-181.
55. Zatta AJ, Kin H, Yoshishige D, Jiang R, Wang N, Reeves JG, Mykytenko J, Guyton RA, Zhao ZQ, Caffrey JL, Vinten-Johansen J (2008) Evidence that cardioprotection by postconditioning involves preservation of myocardial opioid content and selective opioid receptor activation. Am J Physiol Heart Circ Physiol 294: H1444-H1451.
56. Zhang J, Gibney GT, Zhao P, Xia Y (2002) Neuroprotective role of delta-opioid receptors in cortical neurons. AmJ Physiol Cell Physiol 282: C1225-C1234.