The role of fennel on DLK1 gene expression in sheep heart tissue

Document Type : Research Paper

Authors

1 Department of Animal Science, Faculty of Agriculture, College of Agriculture, Shahid Bahonar University of Kerman

2 MSc Student, Animal Science Department, Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran.

3 MSc Student, Animal Science Department, Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran

4 Assistant professor, Department of Biology, Faculty of Science, Shahid Bahonar University of Kerman, Kerman, Iran.

5 Key Laboratory of Animal Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China

Abstract

Objective
Fennel in animal diets for various purposes including improving weight gain, oxidative quality of meat, digestion and growth efficiency, closed cell volume, small intestine length and weight, carcass efficiency, feed intake, red blood cells and hemoglobin count, feed conversion, efficiency and health status and reduction of the total number of bacteria have been used. On the other hand, the DLK1 gene plays an important role in controlling various processes throughout the fetus and adulthood. Therefore, this study aimed to investigate the effect of fennel on DLK1 gene expression in Kermani sheep heart using real-time PCR.
Materials and Methods
In this study, 30 male Kermani lambs (6-month-old) with almost the same weight were selected and randomly divided into three experimental groups (10 in each group). Experimental animals were fed freely and separately with three levels of fennel (0, 1, and 2%) for three months. After slaughtering, the heart weight and fat around the heart were measured and the heart tissue was sampled. RNA extraction and cDNA synthesis were performed using standard kits. The expression of DLK1 genes (target gene) and beta-actin gene (reference gene) was performed using proper primers using real-time PCR method and the results were analyzed with the appropriate software.
Results
The results of the quality assay of extracted RNAs on agarose gel and at A260 / A280 wavelength showed the good quality of total RNA. The results of real-time PCR and electrophoresis of PCR products on agarose gel showed that the DLK1 gene was expressed in heart tissue. Adding fennel to the diet did not significantly change the weight of the heart and the weight of fat around the heart compared to the control diet. The results showed that fennel nutrition at 1% and 2% levels significantly (P <0.05) increased DLK1 gene expression in heart tissue.
Conclusions
Based on the results, it can be concluded that fennel can be used in sheep diet to improve heart structure through positive effects on DLK1 gene expression. Since fennel has increased the expression level of the DLK1 gene in heart tissue, it can be considered to improve heart function. It can be concluded that fennel can be used for different purposes in livestock, but for each effect in each tissue, more research should be done considering different genetic, epigenetic, and physiological conditions to reach a distinct conclusion.

Keywords


محمدآبادی محمدرضا (1399) بیان ژن ESR1 در بز کرکی راینی با استفاده از real time PCR‎. مجله بیوتکنولوژی کشاورزی 12(1)، 192-177.
محمدآبادی محمدرضا (1399) پروفایل بیانی mRNA مختص بافت ژن ESR2  در بز‎. مجله بیوتکنولوژی کشاورزی 12(2)، 184-169.
محمدآبادی محمدرضا، کرد محبوبه، نظری محمود (1397) مطالعه بیان ژن لپتین در بافت‌های مختلف گوسفند کرمانی با استفاده از real time PCR. مجله بیوتکنولوژی کشاورزی 10(3)، 122-111. 
محمدی فر آمنه، محمدآبادی محمدرضا (1390) کاربرد نشانگرهای ریزماهواره برای مطالعه ژنوم گوسفند کرمانی. مجله علوم دا‌می‌ایران 42(4)، 344-337.
References
Abdallah BM, Jensen CH, Gutierrez G, et al. (2004) Regulation of human skeletal stem cells differentiation by DLK1/Pref-1. J Bone Miner Res 19, 841–852.
Aćimović MG, Ljiljana M, Kostadinović NM, et al. (2016) Phytochemical constituents of selected plants from apiaceae family and their biological effects in poultry. Food Feed Res 43, 35-41.
Amiri Roudbar M, Mohammadabadi MR, Mehrgardi AA, Abdollahi-Arpanahi A (2017) Estimates of variance components due to parent-of-origin effects for body weight in Iran-Black sheep. Small Rum Res 149, 1-5.
Amiri Roudbar M., Abdollahi-Arpanahi R., Ayatollahi Mehrgardi A., et al. (2018) Estimation of the variance due to parent-of-origin effects for productive and reproductive traits in Lori-Bakhtiari sheep. Small Rumin Res 160, 95-102.
Badgujar SB, Patel VV, Bandivdekar AH (2014) Foeniculum vulgareMill: a review of its botany, phytochemistry, pharmacology, contemporary application, and toxicology. Biomed Res Int 2014, 1-32.
Bujak M, Frangogiannis NG (2007) The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc Res 74, 184–195.
Charalambous M, Da Rocha ST, Radford EJ, et al. (2014) DLK1/PREF1 regulates nutrient metabolism and protects from steatosis. Proc Natl Acad Sci 111, 16088–16093.
Chen L, Qanie D, Jafari A, et al. (2011) Delta-like 1/fetal antigen-1 (DLK1/FA1) is a novel regulator of chondrogenic cell differentiation via inhibition of the Akt kinase-dependent pathway. J Biol Chem 286, 32140–32149.
Chenani H, Nazari M, Nassiri MTB, et al. (2021) Exonic SNP in MHC-DMB2 is associated with gene expression and humoral immunity in Japanese quails. Vet Immunol Immunopathol 239, e110302.
Driesen RB, Nagaraju CK, Abi-Char J, et al. (2014) Reversible and irreversible differentiation of cardiac fibroblasts. Cardiovasc Res 101, 411–422.
EL-Deek AA, Attia YA, Hannfy MM (2003) Effect of anise (Pimpinella anisiumj), ginger (Zingiber officinale roscoe) and fennel (Foeniculum vulgare) and their mixture of performance of Broilers. Arch Geflugelk 67, 92-96.
Ferron SR, Charalambous M, Radford E, et al. (2011) Postnatal loss of DLK1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature 475, 381–385.
Gharaghani H, Shariatmadari F, Torshizi K (2013) Comparison of oxidative quality of meat of chickens feed corn or wheat based diets with fennel (Foeniculum vulgare Mill.), antibiotic and probiotic as feed additive, under different storage conditions. Archiv Fur Geflugelkunde 77, 199-205.
Ghotbaldini H., Mohammadabadi M.R., Nezamabadi-pour H., et al. (2019). Predicting breeding value of body weight at 6-month age using Artificial Neural Networks in Kermani sheep breed. Acta Scientiarum. Anim Sci 41, e45282.
Hajalizadeh Z, Dayani O, Khezri A, et al. (2019) The effect of adding fennel (Foeniculum vulgare) seed powder to the diet of fattening lambs on performance, carcass characteristics and liver enzymes, Small Rumin Res 175, 72-77.
Karami M, Alimon AR, Yong MG, et al. (2010) Effects of dietary herbal antioxidants supplemented on feedlot growth performance and carcass composition of male goats. Am J Anim Vet Sci 5, 33-39.
Khazaei M, Montaseri A, Khazaei MR, Khanahmadi M. (2011) Study of Foeniculum vulgare Effect on Folliculogenesis in Female Mice. Int J Fertil Steril 5(3), 122-127
Kocher O, Kennedy SP, Madri JA (1990) Alternative splicing of endothelial cell fibronectin mRNA in the IIICS region. Functional significance. Am J Pathol 137, 1509–1524.
Laborda J (2000) The role of the epidermal growth factor-like protein dlk in cell differentiation. Histol Histopathol 15, 119–129.
Li RK, Li G, Mickle DA, et al. (1997) Overexpression of transforming growth factor-beta1 and insulinlike growth factor-I in patients with idiopathic hypertrophic cardiomyopathy. Circulation 96, 874–881.
Lottrup G, Nielsen JE, Skakkebæk NE, et al. (2015) Abundance of DLK1, differential expression of CYP11B1, CYP21A2 and MC2R, and lack of INSL3 distinguish testicular adrenal rest tumours from leydig cell tumours. Eur J Endocrinol 172, 491–499. 
Lui JC, Finkielstain GP, Barnes KM, Baron J (2008) An imprinted gene network that controls mammalian somatic growth is down-regulated during postnatal growth deceleration in multiple organs. Am J Physiol – Regul Integr Comp Physiol 295, R189-196.
Masoudzadeh SH, Mohammadabadi M, Khezri A, et al. (2020a) Effects of diets with different levels of fennel (Foeniculum vulgare) seed powder on DLK1 gene expression in brain, adipose tissue, femur muscle and rumen of Kermani lambs. Small Rumin Res 193, e106276.
Masoudzadeh SH, Mohammadabadi MR, Khezri A, et al. (2020b) DLK1 Gene Expression in Different Tissues of Lamb. Iran J Appl Anim Sci 10 (4), 669-677. 
Mohammadabadi M, Bordbar F, Jensen J, et al. (2021) Key genes regulating skeletal muscle development and growth in farm animals. Animals 11 (3), e8.35.
Mohammadabadi M, Masoudzadeh SH, Khezri A, et al. (2021) Fennel (Foeniculum vulgare) seed powder increases Delta-Like Non-Canonical Notch Ligand 1 gene expression in testis, liver, and humeral muscle tissues of growing lambs. Heliyon 7 (12), e08542.
Mohammadabadi MR (2017) Inter-Simple Sequence Repeat loci Associations with Predicted Breeding Values of Body Weight in Kermani Sheep. Genet 3rd Millen 14 (4), 4383-4390.
Mohammadabadi MR (2020) Expression of ESR1 gene in Raini Cashmere goat using real time PCR. Agric Biotechnol J 12 (1), 177-192 (In Persian).
Mohammadabadi MR (2021) Tissue-specific mRNA expression profile of ESR2 gene in goat. Agricultural Biotechnology Journal 12 (4), 169-184 (In Persian).
Mohammadabadi MR, Esfandyarpoor E, Mousapour A (2017) Using Inter Simple Sequence Repeat Multi-Loci Markers for Studying Genetic Diversity in Kermani Sheep. Journal of Research and Development 5 (2), e154.
Mohammadabadi MR, Kord M, Nazari M (2018) Studying expression of leptin gene in different tissues of Kermani Sheep using Real Time PCR. Journal of Agricultural Biotechnology 10 (3), 111-122 (In Persian).
Mohammadifar A, Mohammadabadi MR (2011) Application of Microsatellite Markers for a Study of Kermani Sheep Genome. Iran J Anim Sci 42 (4), 337-344 (In Persian).
Mohammed A, Abbas R (2009) The effect of using fennel seeds (Foeniculum vulgare L.) on productive performance of broiler chickens. Int J Poult Sci 8, 642-644.
Moon YS, Smas CM, Lee K (2002) Mice lacking paternally expressed Pref-1/DLK1 display growth retardation and accelerated adiposity. Mol Cell Biol 22, 5585–5592.
Oczkowicz M, Piestrzyska-Kajtoch A, Piórkowska K, et al. (2010) Expression of DLK1 and MEG3 genes in porcine tissues during postnatal development. Genet Mol Biol 33, 790-794. 
Rather MA, Dar BA, Sofi SN, et al. (2016) Foeniculum vulgare: A comprehensive review of its traditional use, phytochemistry, pharmacology, and safety. Arab J Chem 9, S1574-S1583.
Rocha ST, Tevendale M, Knowles E, et al. (2007) Restricted co-expression of DLK1 and the reciprocally imprinted non-coding RNA, Gtl2: Implications for cis-acting control. Dev Biol, 306, 810–823. 
Rodriguez P, Sassi Y, Troncone L, et al. (2019) Deletion of delta-like 1 homologue accelerates fibroblast–myofibroblast differentiation and inducesmyocardial fibrosis. Eur Heart J 40, 967–978.
Sakajiri S, O’Kelly J, Yin D, et al. (2005) DLK1 in normal and abnormal hematopoiesis. Leukemia 19, 1404–1410. 
Serini G, Bochaton-Piallat ML, Ropraz P, et al. (1998) The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1. J Cell Biol 142, 873–881.
Shahsavari M, Mohammadabadi M, Khezri A, et al. (2021) Correlation between insulin-like growth factor 1 gene expression and fennel (Foeniculum vulgare) seed powder consumption in muscle of sheep. Animal Biotechnology 33, 1-11.
Sotoudeh A, Yeganeh S (2016) Effects of supplementary fennel (Foeniculum vulgare) essential oil in diet on growth and reproductive performance of the ornamental fish, Convict cichlid (Cichlasoma nigrofasciatum). Aquacul Res 2016, 1–8.
Tanimizu N, Nishikawa M, Saito H, et al. (2003) Isolation of hepatoblasts based on the expression of dlk/pref-1. J Cell Sci 116, 1775-1786. 
Travers JG, Kamal FA, Robbins J, et al. (2016) Cardiac fibrosis: the fibroblast awakens. Circ Res 118, 1021–1040.
Waddell JN, Zhang P, Wen Y, et al. (2010) DLK1 is necessary for proper skeletal muscle development and regeneration, PLoS One 5, 1–12. 
Yevtodiyenko A, Schmidt JV (2006) DLK1 expression marks developing endothelium and sites of branching morphogenesis in the mouse embryo and placenta. Dev Dyn 235, 1115–1123.