https://doi.org/10.4081/ejh.2023.3890
Investigation of seasonal changes in lipid synthesis and metabolism-related genes in the oviduct of Chinese brown frog (Rana dybowskii)
Submitted: 17 October 2023
Accepted: 9 December 2023
Published: 20 December 2023
Accepted: 9 December 2023
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
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A peculiar physiological characteristic of the Chinese brown frog (Rana dybowskii) is that its oviduct dilates during pre-brumation rather than during the breeding season. This research aimed to examine the expression of genes connected with lipid synthesis and metabolism in the oviduct of R. dybowskii during both the breeding season and pre-brumation. We observed significant changes in the weight and size of the oviduct between the breeding season and pre-brumation. Furthermore, compared to the breeding season, pre-brumation exhibited significantly lower triglyceride content and a marked increase in free fatty acid content. Immunohistochemical results revealed the spatial distribution of triglyceride synthase (Dgat1), triglyceride hydrolase (Lpl and Hsl), fatty acid synthase (Fasn), and fatty acid oxidases (Cpt1a, Acadl, and Hadh) in oviductal glandular cells and epithelial cells during both the breeding season and pre-brumation. While the mRNA levels of triglycerides and free fatty acid synthesis genes (dgat1 and fasn) did not show a significant difference between the breeding season and pre-brumation, the mRNA levels of genes involved in triglycerides and free fatty acid metabolism (lpl, cpt1a, acadl, acox and hadh) were considerably higher during pre-brumation. Furthermore, the R. dybowskii oviduct's transcriptomic and metabolomic data confirmed differential expression of genes and metabolites enriched in lipid metabolism signaling pathways during both the breeding season and pre-brumation. Overall, these results suggest that alterations in lipid synthesis and metabolism during pre-brumation may potentially influence the expanding size of the oviduct, contributing to the successful overwintering of R. dybowskii.
Niu Y, Cao W, Storey KB, He J, Wang J, Zhang T, et al. Metabolic characteristics of overwintering by the high-altitude dwelling Xizang plateau frog, Nanorana parkeri. J Comp Physiol B 2020;190:433-44.
DOI: https://doi.org/10.1007/s00360-020-01275-4
Fan C, Liu Y, Wang Y, Zhang A, Xie W, Zhang H, et al. Expression of glycogenic genes in the oviduct of Chinese brown frog (Rana dybowskii) during pre-brumation. Theriogenology 2022;185:78-87.
DOI: https://doi.org/10.1016/j.theriogenology.2022.03.006
Wang H, Zhou N, Zhang R, Wu Y, Zhang R, Zhang S. Identification and localization of gastrointestinal hormones in the skin of the bullfrog Rana catesbeiana during periods of activity and hibernation. Acta Histochem 2014;116:1418-26.
DOI: https://doi.org/10.1016/j.acthis.2014.09.005
Green SR, Storey KB. Functional and post-translational characterization of pyruvate dehydrogenase demonstrates repression of activity in the liver but not skeletal muscle of the Richardson's ground squirrel (Urocitellus richardsonii) during hibernation. J Therm Biol 2021;99:102996.
DOI: https://doi.org/10.1016/j.jtherbio.2021.102996
Scott DE, Casey ED, Donovan MF, Lynch TK. Amphibian lipid levels at metamorphosis correlate to post-metamorphic terrestrial survival. Oecologia 2007;153:521-32.
DOI: https://doi.org/10.1007/s00442-007-0755-6
Otis JP, Sahoo D, Drover VA, Yen CL, Carey HV. Cholesterol and lipoprotein dynamics in a hibernating mammal. PLoS One 2011;6:e29111.
DOI: https://doi.org/10.1371/journal.pone.0029111
Lin JQ, Huang YY, Bian MY, Wan QH, Fang SG. A unique energy-saving strategy during hibernation revealed by multi-omics analysis in the Chinese alligator. iScience 2020;23:101202.
DOI: https://doi.org/10.1016/j.isci.2020.101202
Rosner E, Voigt CC. Oxidation of linoleic and palmitic acid in pre-hibernating and hibernating common noctule bats revealed by 13C breath testing. J Exp Biol 2018;221:jeb168096.
DOI: https://doi.org/10.1242/jeb.168096
Ensminger DC, Salvador-Pascual A, Arango BG, Allen KN, Vázquez-Medina JP. Fasting ameliorates oxidative stress: A review of physiological strategies across life history events in wild vertebrates. Comp Biochem Physiol A Mol Integr Physiol 2021;256:110929.
DOI: https://doi.org/10.1016/j.cbpa.2021.110929
Wang G, Kim WK, Cline MA, Gilbert ER. Factors affecting adipose tissue development in chickens: A review. Poult Sci 2017;96:3687-99.
DOI: https://doi.org/10.3382/ps/pex184
Costanzo JP. Overwintering adaptations and extreme freeze tolerance in a subarctic population of the wood frog, Rana sylvatica. J Comp Physiol B 2019;189:1-15.
DOI: https://doi.org/10.1007/s00360-018-1189-7
Maurya RK, Bharti S, Krishnan MY. Triacylglycerols: Fuelling the Hibernating Mycobacterium tuberculosis. Front Cell Infect Microbiol 2019;8:450.
DOI: https://doi.org/10.3389/fcimb.2018.00450
Nielsen TS, Jessen N, Jørgensen JO, Møller N, Lund S. Dissecting adipose tissue lipolysis: molecular regulation and implications for metabolic disease. J Mol Endocrinol 2014;52:R199-222.
DOI: https://doi.org/10.1530/JME-13-0277
Tan QQ, Liu W, Zhu F, Lei CL, Wang XP. Fatty acid synthase 2 contributes to diapause preparation in a beetle by regulating lipid accumulation and stress tolerance genes expression. Sci Rep 2017;7:40509.
DOI: https://doi.org/10.1038/srep40509
Chitraju C, Mejhert N, Haas JT, Diaz-Ramirez LG, Grueter CA, Imbriglio JE, et al. Triglyceride synthesis by DGAT1 protects adipocytes from lipid-induced ER stress during lipolysis. Cell Metab 2017;26:407-18.e3.
DOI: https://doi.org/10.1016/j.cmet.2017.07.012
Lin H, Liu Z, Yang H, Lu L, Chen R, Zhang X, et al. Per- and polyfluoroalkyl substances (PFASs) impair lipid metabolism in Rana nigromaculata: A field investigation and laboratory study. Environ Sci Technol 2022;56:13222-32.
DOI: https://doi.org/10.1021/acs.est.2c03452
Frühbeck G, Méndez-Giménez L, Fernández-Formoso JA, Fernández S, Rodríguez A. Regulation of adipocyte lipolysis. Nutr Res Rev 2014;27:63-93.
DOI: https://doi.org/10.1017/S095442241400002X
Prieto D, Oppezzo P. Lipoprotein lipase expression in chronic lymphocytic leukemia: New insights into leukemic progression. Molecules 2017;22:2083.
DOI: https://doi.org/10.3390/molecules22122083
Steensels S, Ersoy BA. Fatty acid activation in thermogenic adipose tissue. Biochim Biophys Acta Mol Cell Biol Lipids 2019;1864:79-90.
DOI: https://doi.org/10.1016/j.bbalip.2018.05.008
Li Z, Zhang H. Reprogramming of glucose, fatty acid and amino acid metabolism for cancer progression. Cell Mol Life Sci 2016;73:377-92.
DOI: https://doi.org/10.1007/s00018-015-2070-4
Simcox J, Geoghegan G, Maschek JA, Bensard CL, Pasquali M, Miao R, et al. Global analysis of plasma lipids identifies liver-derived acylcarnitines as a fuel source for brown fat thermogenesis. Cell Metab 2017;26:509-22.e6.
DOI: https://doi.org/10.1016/j.cmet.2017.08.006
Schlaepfer IR, Joshi M. CPT1A-mediated fat oxidation, mechanisms, and therapeutic potential. Endocrinology 2020;161:bqz046.
DOI: https://doi.org/10.1210/endocr/bqz046
Li A, Li Y, Wang Y, Wang Y, Li X, Qubi W, et al. ACADL promotes the differentiation of goat intramuscular adipocytes. Animals 2023;13:281.
DOI: https://doi.org/10.3390/ani13020281
Joo HJ, Kim KY, Yim YH, Jin YX, Kim H, Kim MY, Paik YK. Contribution of the peroxisomal acox gene to the dynamic balance of daumone production in Caenorhabditis elegans. J Biol Chem 2010;285:29319-25.
DOI: https://doi.org/10.1074/jbc.M110.122663
Shen YQ, Lang BF, Burger G. Diversity and dispersal of a ubiquitous protein family: acyl-CoA dehydrogenases. Nucleic Acids Res 2009;37:5619-31.
DOI: https://doi.org/10.1093/nar/gkp566
Li M, Wang Y, Tang Z, Wang H, Hu J, Bao Z, Hu X. Expression plasticity of peroxisomal acyl-coenzyme A oxidase genes implies their involvement in redox regulation in scallops exposed to PST-producing Alexandrium. Mar Drugs 2022;20:472.
DOI: https://doi.org/10.3390/md20080472
Fang H, Li H, Zhang H, Wang S, Xu S, Chang L, et al. Short-chain L-3-hydroxyacyl-CoA dehydrogenase: A novel vital oncogene or tumor suppressor gene in cancers. Front Pharmacol 2022;13:1019312.
DOI: https://doi.org/10.3389/fphar.2022.1019312
Olsen L, Thum E, Rohner N. Lipid metabolism in adaptation to extreme nutritional challenges. Dev Cell 2021;56:1417-29.
DOI: https://doi.org/10.1016/j.devcel.2021.02.024
Shen Y, Liu Y, Ma J, Ma X, Tian Y, Zhang H, et al. Immunoreactivity of c-kit receptor protein during the pre-hibernation period in the oviduct of the Chinese brown frog, Rana chensinensis. J Vet Med Sci 2012;74:209-13.
DOI: https://doi.org/10.1292/jvms.11-0033
Xi L, Wang C, Chen P, Yang Q, Hu R, Zhang H, et al. Expressions of IL-6, TNF-α and NF-κB in the skin of Chinese brown frog (Rana dybowskii). Eur J Histochem 2017;61:2834.
DOI: https://doi.org/10.4081/ejh.2017.2834
Hu R, Xi L, Cao Q, Yang R, Liu Y, Sheng X, et al. The expression of prostaglandin-E2 and its receptor in the oviduct of Chinese brown frog (Rana dybowskii). Prostaglandins Other Lipid Mediat 2016;124:9-15.
DOI: https://doi.org/10.1016/j.prostaglandins.2016.05.006
Tang Z, Chen Y, Ren B, Wang X, Zhang H, Han Y, et al. Immunoreactivities of AR, ERα, ERβ and aromatase in the nuptial pad of Chinese brown frog (Rana dybowskii) during pre-hibernation and the breeding period. Eur J Histochem 2021;65:3206.
DOI: https://doi.org/10.4081/ejh.2021.3206
Zhang Y, Zhang A, Zhao Y, Feng X, Sheng Y, Zhang H, et al. Expressions of TLR4, MyD88, IRAK4 and NF-κB in the oviduct of Chinese brown frog (Rana dybowskii). Eur J Histochem 2019;63:3050.
DOI: https://doi.org/10.4081/ejh.2019.3050
Liu Y, Weng J, Huang S, Shen Y, Sheng X, Han Y, et al. Immunoreactivities of PPARγ2, leptin and leptin receptor in oviduct of Chinese brown frog during breeding period and pre-hibernation. Eur J Histochem 2014;58:2422.
DOI: https://doi.org/10.4081/ejh.2014.2422
Guo X, Wang Z, Liu L, Li Y. Transcriptome and metabolome analyses of cold and darkness-induced pellicle cysts of Scrippsiella trochoidea. BMC Genomics 2021;22:526.
DOI: https://doi.org/10.1186/s12864-021-07840-7
Wang W, Pang J, Zhang F, Sun L, Yang L, Zhao Y, et al. Integrated transcriptomics and metabolomics analysis to characterize alkali stress responses in canola (Brassica napus L.). Plant Physiol Biochem 2021;166:605-20.
DOI: https://doi.org/10.1016/j.plaphy.2021.06.021
Zhang J, Jiang C, Liu X, Jiang CX, Cao Q, Yu B, et al. The metabolomic profiling identifies N, N-dimethylglycine as a facilitator of dorsal root ganglia neuron axon regeneration after injury. FASEB J 2022;36:e22305.
DOI: https://doi.org/10.1096/fj.202101698R
Lin DM, Chen XJ, Wei, YR, Chen Y. The energy accumulation of somatic tissue and reproductive organs in post-recruit female Illex argentinus and the relationship with sea surface oceanography. Fish Res 2017;185:102-114.
DOI: https://doi.org/10.1016/j.fishres.2016.09.023
Abdul-Rahman II, Obese FY, Robinson JE, Awumbila B, Jeffcoate IA. Effects of season on the reproductive organs and steroid hormone profiles in guinea hens (Numida meleagris). Br Poult Sci 2016;57:280-6.
DOI: https://doi.org/10.1080/00071668.2016.1154504
Hurley LL, Crino OL, Rowe M, Griffith SC. Variation in female reproductive tract morphology across the reproductive cycle in the zebra finch. PeerJ 2020;8:e10195.
DOI: https://doi.org/10.7717/peerj.10195
Huang Y, Chen H, Yang P, Bai X, Shi Y, Vistro WA, et al. Hepatic lipid droplet breakdown through lipolysis during hibernation in Chinese Soft-Shelled Turtle (Pelodiscus sinensis). Aging (Albany NY) 2019;11:1990-2002.
DOI: https://doi.org/10.18632/aging.101887
Ren Y, Song S, Liu X, Yang M. Phenotypic changes in the metabolic profile and adiponectin activity during seasonal fattening and hibernation in female Daurian ground squirrels (Spermophilus dauricus). Integr Zool 2022;17:297-310.
DOI: https://doi.org/10.1111/1749-4877.12504
Yan J, Burman A, Nichols C, Alila L, Showe LC, Showe MK, et al. Detection of differential gene expression in brown adipose tissue of hibernating arctic ground squirrels with mouse microarrays. Physiol Genomics 2006;25:346-53.
DOI: https://doi.org/10.1152/physiolgenomics.00260.2005
Watts AJ, Logan SM, Kübber-Heiss A, Posautz A, Stalder G, Painer J, et al. Regulation of peroxisome proliferator-activated receptor pathway during torpor in the Garden dormouse, Eliomys quercinus. Front Physiol 2020;11:615025.
DOI: https://doi.org/10.3389/fphys.2020.615025
Xiong S, Wang W, Kenzior A, Olsen L, Krishnan J, Persons J, et al. Enhanced lipogenesis through PPARγ helps cavefish adapt to food scarcity. Curr Biol 2022;32:2272-80.e6.
DOI: https://doi.org/10.1016/j.cub.2022.03.038
Niu Y, Cao W, Wang J, He J, Storey KB, Ding L, et al. Freeze tolerance and the underlying metabolite responses in the Xizang plateau frog, Nanorana parkeri. J Comp Physiol B 2021;191:173-84.
DOI: https://doi.org/10.1007/s00360-020-01314-0
Rice SA, Mikes M, Bibus D, Berdyshev E, Reisz JA, Gehrke S, Bronova I, et al. Omega 3 fatty acids stimulate thermogenesis during torpor in the Arctic Ground Squirrel. Sci Rep 2021;11:1340.
DOI: https://doi.org/10.1038/s41598-020-78763-8
Vuarin P, Henry PY, Guesnet P, Alessandri JM, Aujard F, Perret M, Pifferi F. Shallow hypothermia depends on the level of fatty acid unsaturation in adipose and liver tissues in a tropical heterothermic primate. J Therm Biol 2014;43:81-8.
DOI: https://doi.org/10.1016/j.jtherbio.2014.05.002
Jackson DC, Ultsch GR. Physiology of hibernation under the ice by turtles and frogs. J Exp Zool A Ecol Genet Physio. 2010;313:311-27.
DOI: https://doi.org/10.1002/jez.603
Do Amaral MCF, Frisbie J, Goldstein DL, Krane CM. The cryoprotectant system of Cope’s gray treefrog, Dryophytes chrysoscelis: responses to cold acclimation, freezing, and thawing. J Comp Physiol B 2018;188:611-21.
DOI: https://doi.org/10.1007/s00360-018-1153-6
Ethics Approval
All animal testing procedures were approved by the Animal Protection and Utilization Policy of the Beijing Forestry University Ethics CommitteeSupporting Agencies
Beijing Natural Science Foundation, National Natural Science Foundation of ChinaHow to Cite
Wang, Y., Liu, Y., Wang, Y., Zhang, A., Xie, W., Zhang, H., … Xu, M. (2023). Investigation of seasonal changes in lipid synthesis and metabolism-related genes in the oviduct of Chinese brown frog (<em>Rana dybowskii</em>). European Journal of Histochemistry, 67(4). https://doi.org/10.4081/ejh.2023.3890
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