Dlk1 Gene Expression in Different Tissues of Lamb

الموضوعات :

S.H. Masoudzadeh ¹ (Department of Animal Science, Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran)
M.R. Mohammadabadi ² (Department of Animal Science, Shahid Bahonar University of Kerman, Kerman, Iran)
A. Khezri ³ (Department of Animal Science, Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran)
O.A. Kochuk-Yashchenko ⁴ (Department of Breeding, Animal Genetics and Biotechnology, Zhytomyr National Agroecological University, Zhytomyr, Ukraine)
D.M. Kucher ⁵ (Department of Breeding, Animal Genetics and Biotechnology, Zhytomyr National Agroecological University, Zhytomyr, Ukraine)
O.I. Babenko ⁶ (Department of Animal Science, Bila Tserkva National Agrarian University, BilaTserkva, Ukraine)
M.V. Bushtruk ⁷ (Department of Animal Science, Bila Tserkva National Agrarian University, BilaTserkva, Ukraine)
S.V. Tkachenko ⁸ (Department of Animal Science, Bila Tserkva National Agrarian University, BilaTserkva, Ukraine)
R.V. Stavetska ⁹ (Department of Animal Science, Bila Tserkva National Agrarian University, BilaTserkva, Ukraine)
N.I. Klopenko ¹⁰ (Department of Animal Science, Bila Tserkva National Agrarian University, BilaTserkva, Ukraine)
V.P. Oleshko ¹¹ (Department of Animal Science, Bila Tserkva National Agrarian University, BilaTserkva, Ukraine)
M.V. Tkachenko ¹² (Department of Animal Science, Bila Tserkva National Agrarian University, BilaTserkva, Ukraine)
I.V. Titarenko ¹³ (Department of Animal Science, Bila Tserkva National Agrarian University, BilaTserkva, Ukraine)

تاريخ الإرسال : 13 الثلاثاء , ربيع الثاني, 1441 تاريخ التأكيد : 05 الخميس , جمادى الثانية, 1441 تاريخ الإصدار : 16 الثلاثاء , ربيع الثاني, 1442

الکلمات المفتاحية: expression, lamb, Real-time PCR, Tissues, Dlk1,

ملخص المقالة :

Delta-like 1 homolog or pre-adipocyte factor 1 (Dlk1) is one of the most significant genes and widely expresses all over mammal’s development. Some of the functions identified for Dlk1gene are development of muscle, healing of wound, adipocytes proliferation, liver, lung and pancreas development. It also prevents Notch gene conducting toward to govern several operations such like cellular proliferation and differentiation. The aim of this study was to assay the expression of Dlk1 gene in liver, humeral and femur muscles, brain, adipose, testis and rumen tissues of Kermani lambs. Tissue samples from thirty male lambs of Kermani sheep with approximately the similar weight and age from the Animal Science Research and Training Station of Shahid Bahonar University of Kerman were picked up. Total RNA was isolated, cDNA was synthesized and Real-Time PCR was performed. SAS and REST softwares were used for analyzing the results. The Dlk1 gene was expressed in all studied tissues of Kermani sheep. The highest expression of Dlk1 gene expression was observed in liver tissue. There was no statistically significant difference between rumen and femur (leg) muscle, between humeral muscle and liver and between adipose and brain tissue (P>0.05). The lowest expression was related to testicular tissue. Based on results of current study, it can be concluded that this gene has pleiotropic effects with different major and minor outcomes in different tissues. But, for reaching to more decisive conclusion for any tissue, it is necessary to carry out further research noticing various physiological, epigenetic and genetic conditions.

المصادر:

Ahsani M.R., Bafti M.S., Esmailizadeh A.K. and Mohammadabadi M.R. (2011). Genotyping of isolates of Clostridium perfringens from vaccinated and unvaccinated sheep. Small Rumin. Res. 95, 65-69.

Ahsani M.R., Mohammadabadi M.R. and Shamsaddini M.B. (2010). Clostridium perfringens isolate typing by multiplex PCR. J. Venom. Anim. Toxin Incl. Trop. Dis. 16, 573-578.

Amiri Roudbar M., Abdollahi-Arpanahi R., Ayatollahi Mehrgardi A., Mohammadabadi M., Taheri Yeganeh A. and Rosa G.J.M. (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.

Andersen D.C., Petersson S.J., Jørgensen L.H., Bollen P., Jensen P.B., Teisner B., Schroeder H.D. and Jensen C.H. (2009). Characterization of Dlk1+ Cells emerging during skeletal muscle remodeling in response to myositis, myopathies, and acute injury. Stem Cell. 27, 898-908.

Baladrón V., Ruiz-Hidalgo M.J., Nueda M.L., Díaz-Guerra M.J.M., García-Ramírez J.J., Bonvini E., Gubina E. andLabord J. (2005). DLK acts as a negative regulator of Notch1 activation through interactions with specific EGF-like repeats. Exp. Cell Res. 303, 343-359.

Bauer S.R., Ruiz-Hidalgo M.J., Rudikoff E.K., Goldstein J. andLaborda J. (1998). Modulated expression of the epidermal growth factor-like homeotic protein dlk influences stromal-cell-pre-B-cell interactions, stromal cell adipogenesis, and pre-B-cell interleukin-7 requirements. Mol. Cell. Biol. 18, 5247-5255.

Bujak E., Ritz D. and Neri D. (2015). A monoclonal antibody to human Dlk1 reveals differential expression in cancer and absence in healthy tissues. Antibodies. 4, 71-87.

Charalambous M., Da Rocha S.T., Radford E.J., Medina-Gomez G., Curran S., Pinnock S.B., Ferrón S.R., Vidal-Puig A. and Ferguson-Smith A.C. (2014). Dlk1/PREF1 regulates nutrient metabolism and protects from steatosis. Proc. Natl Acad Sci. 111, 16088-16093.

Cockett N.E., Jackson S.P., Shay T.L., Farnir F., Berghmans S., Snowder G.D., Nielsen D.M. and Georges M. (1996). Polar overdominance at the ovine callipyge locus. Science. 273, 236-238.

Davis E., Caiment F., Tordoir X., Cavaille J. and Ferguson-Smith A. (2005). RNAi-mediated allelic trans-Interaction at the imprinted Rtl1/Peg11 Locus. Curr. Biol. 15, 743-749.

Deiuliis J.A., Li B., Lyvers-Peffer P.A., Moeller S.J. and Lee K. (2006). Alternative splicing of delta-like 1 homolog (Dlk1) in the pig and human. Comp. Biochem. Physiol. B. 145, 50-59.

Falix F.A., Tjon-A-Loi M.R.S., Gaemers I.C., Aronson D.C. andLamers W.H. (2013). Dlk1 protein expression during mouse development provides new insights into its function. ISRN Dev. Biol. 62, 1-10.

Fleming-Waddell J.N., Gayla R.O., Tasia M.T., Jason D.W., Tony V., Bruce A.C., Ross L.T., Mike K.N., Noelle E.C. and Christopher A.B. (2009). Effect of Dlk1 and RTL1 but not MEG3 or MEG8 on muscle gene expression in callipyge lambs. PLoS One. 4, e7399.

Ghotbaldini H., Mohammadabadi M.R., Nezamabadi-pour H., Babenko O.I., Bushtruk M.V. and Tkachenko S.V. (2019). Predicting breeding value of body weight at 6-month age using Artificial Neural Networks in Kermani sheep breed. Acta Sci. Anim. Sci. 41, 1-9.

Harel A., Dalah I., Pietrokovski S., Safran M. and Lancet D. (2011). Omics data management and annotation. Pp. 71-96 in Bioinformatics for Omics Data. B. Mayer, Ed. Humana Press, New York, USA.

Jensen C.H., Krogh T.N., Højrup P., Clausen P.P., Skjødt K., Larsson L.I., Enghild J.J. and Teisner B. (1994). Protein structure of fetal antigen 1 (FA1). European J. Biochem. 225, 83-92.

Jensen C.H., Teisner B., Højrup P., Rasmussen H.B., Madsen O.D., Nielsen B. and Skjødt K. (1993). Studies on the isolation, structural analysis and tissue localization of fetal antigen 1 and its relation to a human adrenal-specific cDNA, pG2. Hum. Reprod. 8, 635-641.

Kaneta M., Osawa M., Sudo K., Nakauchi H., Farr A.G. and Takahama Y. (2000). A role for pref-1 and HES-1 in thymocyte development. J. Immunol. 164, 256-264.

Kawakami T., Tokuhiro C., Kahori M., Hidetoshi O., Yusaku O. and Keisei O. (2006). Imprinted Dlk1 is a putative tumor suppressor gene and inactivated by epimutation at the region upstream of GTL2 in human renal cell carcinoma. Hum. Mol. Genet. 15, 821-830.

Khodabakhshzadeh R., Mohammadabadi M.R., Esmailizadeh A.K., Moradi-Shahrebabak H., Bordbar F. and Ansari Namin S. (2016). Identification of point mutations in exon 2 of GDF9 gene in Kermani sheep. Polish J. Vet. Sci. 19, 281-289.

Kim K.S., Kim J.J., Dekkers J.C. and Rothschild M.F. (2004). Polar overdominant inheritance of a Dlk1 polymorphism is associated with growth and fatness in pigs. Mamm. Genome.15, 552-559.

Li X.P., Do K.T., Kim J.J., Huang J., Zhao S.H., Lee Y., Rothschild M.F., Lee C.K. and Kim K.S. (2008). Molecular characteristics of the porcine Dlk1 and MEG3 genes. Anim. Genet. 39, 189-192.

Lottrup G., Nielsen J.E., Maroun L.L., Møller L.M.A., Yassin M., Leffers H., Skakkebæk N.E. and Rajpert-De Meyts E. (2014). Expression patterns of Dlk1 and INSL3 identify stages of leydig cell differentiation during normal development and in testicular pathologies, including testicular cancer and klinefelter syndrome. Hum. Reprod. 19, 1-14.

Lottrup G., Nielsen J.E., Skakkebæk N.E., Juul A. and Meyts E.R. (2015). Abundance of Dlk1, differential expression of CYP11B1, CYP21A2 and MC2R, and lack of INSL3 distinguish testicular adrenal rest tumours from leydig cell tumours. European J. Endocrinol. 172, 491-499.

Mohammadabadi M.R. (2016). Inter-simple sequence repeat loci associations with predicted breeding values of body weight in Kermani sheep. Genet. 3^rd Millennium. 14, 4383-4390.

Mohammadabadi M.R., Jafari A.H.D. and Bordbar F. (2017). Molecular analysis of CIB4 gene and protein in Kermani sheep. Brazilian J. Med. Biol. Res. 50, 1-9.

Moore K.A., Pytowski B., Witte L., Hicklin D. and Lemischka I.R. (1997). Hematopoietic activity of a stromal cell transmembrane protein containing epidermal growth factor-like repeat motifs. Proc. Natl. Acad. Sci. USA. 94, 4011-4016.

Nueda M.L., Baladrón V., Sánchez-Solana B., Ballesteros M.Á. and Laborda J. (2007). The EGF-like protein Dlk1 inhibits notch signaling and potentiates adipogenesis of mesenchymal cells. J. Mol. Biol. 367, 1281-1293.

Oczkowicz M., Piestrzyska-Kajtoch A., Piórkowska K., Rejduch B. and Rózycki M. (2010). Expression of Dlk1 and MEG3 genes in porcine tissues during postnatal development. Genet. Mol. Biol. 33, 790-794.

Pfaffl M.W., Horgan G.W. and Dempfle L. (2002). Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, 1-36.

Rocha S.T., Tevendale M., Knowles E., Takada S., Watkins M. and Ferguson-Smith A.C. (2007). Restricted co-expression of Dlk1 and the reciprocally imprinted non-coding RNA, Gtl2: Implications for cis-acting control. Dev. Biol. 306, 810-823.

SAS (2005). SAS User’s Guide. SAS Institute Inc Version 9.1. Cary, NC, USA.

Shin J., Velleman S.G., Latshaw J.D., Wick M.P., Suh Y. and Lee K. (2009). The ontogeny of delta-like protein 1 messenger ribonucleic acid expression during muscle development and regeneration: Comparison of broiler and Leghorn chickens. Poult. Sci. 88, 1427-1437.

Smas C.M. and Sul H.S. (1993). Pref-1, a protein containing EGF-like repeats, inhibits adipocyte differentiation. Cell. 73, 725-734.

Smit M., Segers K., Carrascosa L.G., Shay T., Baraldi F., Gyapay G., Snowder G., Georges M., Cockett N. and Charlier C. (2003). Mosaicism of solid gold supports the causality of a noncoding A-to-G transition in the determinism of the callipyge phenotype. Genetics. 163, 453-456.

Soufy B., Mohammadabadi M.R., Shojaeyan K., Baghizadeh A. and Ferasaty S. (2009). Evaluation of myostatin gene polymorphism in Sanjabi sheep by PCR-RFLP method. Anim. Sci. Res. 19, 81-89.

Su R., Sun W., Li D., Wang Q.Z., Lv X.Y., Musa H.H., Chen L., Zhang Y.F. and Wu W.Z. (2014). Association between Dlk1 and IGF-I gene expression and meat quality in sheep. Genet. Mol. Res. 13, 10308-10319.

Surmacz B., Noisa P., Risner-Janiczek J.R., Hui K., Ungless M., Cui W. and Li M. (2012). Dlk1 promotes neurogenesis of human and mouse pluripotent stem cell-derived neural progenitors via modulating Notch and BMP signalling. Stem Cell Rev.Rep. 8, 459-471.

Tanimizu N., Nishikawa M., Saito H., Tsujimura T. and Miyajima A. (2003). Isolation of hepatoblasts based on the expression of dlk/pref-1. J. Cell Sci. 116, 1775-1786.

Traustadottir G.A., Kosmina R., Sheikh S.P., Jensenab C.H. and Andersen D.C. (2013). Preadipocytes proliferate and differentiate under the guidance of Delta-like 1 homolog (Dlk1). Adipocyte. 2, 272-275.

Vajed Ebrahimi M.T., Mohammadabadi M.R. and Esmailizadeh A.K. (2016). Using microsatellite markers to analyze genetic diversity in 14 sheep types in Iran. Arch. Anim. Breed. 60, 183-189.

Yevtodiyenko A. and Schmidt J.V. (2006). Dlk1 expression marks developing endothelium and sites of branching morphogenesis in the mouse embryo and placenta. Dev. Dynam. 235, 1115-1123.

Yin D., Xie D., Sakajiri S., Miller C.W., Zhu H., Popoviciu M.L., Said J.W., Black K.L. and Koeffler H.P. (2006). Dlk1: increased expression in gliomas and associated with oncogenic activities. Oncogene. 25, 1852-1861.

Yuan B., Zhang H., Wang X., Pan Y. and Jiang J. (2018). Effect of nano-SiO₂ on expression and aberrant methylation of imprinted genes in lung and testis. Nanoscale Res. Lett. 13, 266-272.

Zamani P., Akhondi M. and Mohammadabadi M.R. (2015). Associations of inter-simple sequence repeat loci with predicted breeding values of body weight in sheep. Small Rumin. Res. 132, 123-127.

Zamani P., Akhondi M., Mohammadabadi M.R., Banabazi M.H. and Abdolmohammadi A.R. (2011). Genetic variation of mehraban sheep using two intersimple sequence repeat (ISSR) markers. African J. Biotechnol. 10, 1812-1817.