Analysis of the Regulatory Effects of lncRNAs on Kidney Tissue in Ascites Susceptible Broiler

پژوهشهای علوم دامی ایران

Article 6, Volume 16, Issue 2 - Serial Number 58, June 2024, Pages 235-247   

Document Type: Research Articles

DOI: 10.22067/ijasr.2023.83528.1162

Authors

Kasra Ahmadian¹; Mohammadreza Nassiry^{* 2}; Karim Hasanpur³; Ali Javadmanesh⁴

¹Department of Animal Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran.

²Department Animal Science, Faculty of agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

³Department of Animal Science, Faculty of Agriculture, University of Tabriz, Tabriz, Iran

⁴Department of Animal Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Iran.

Abstract

Introduction :Ascites syndrome, as a metabolic disorder, is one of the most non-infectious causes of death in the old age of breeding in the poultry industry, which causes annual losses of over one hundred million dollars and is an important economic concern. The growth rate of broiler and their high need for oxygen causes an increase in pumping, followed by heart failure, and heart failure is often associated with other diseases. Due to the relationship between the heart and the kidney, chronic heart failure leads to a decrease in filtered blood volume and a decrease in kidney function, which over time causes permanent damage to the kidneys. lncRNAs play important roles in a variety of different mechanisms related to cellular homeostasis and in a wide range of pathophysiological processes and pathogenesis of many diseases, including cardiovascular disorders, respiratory and kidney diseases, preliminary studies in human samples show shows that lncRNAs are strongly involved in the development and disease of the kidney. For this reason, the lncRNAs obtained from the RNA-seq data of the kidney tissue were investigated in the occurrence of ascites.
Materials and Methods :700 one-day-old chicks from one of the paternal lines of a commercial strain were kept under standard conditions until 21 days old. On the 21st day of the breeding period, cold stress (24 degrees Celsius) began and continued until the age of 48 days. After applying cold stress, the birds with ascites symptoms were grouped in the Ascites group and the rest in the Healthy group. On the 39th day of the breeding period, 70 slaughtered birds and kidney tissue samples from each bird were immediately transferred to the liquid nitrogen tank after separation. 16 ascites birds and 16 healthy birds were used for RNA extraction. Total RNA extraction was done individually using trizol (YTzol) solution, and then an equal amount of RNA from four tissue samples was combined and then cDNA was prepared from 4 ascites tissue samples and 4 healthy tissue samples. All small RNAs, such as rRNAs, tRNAs, etc., were removed by dt oligo beads, and finally, all mRNAs were used to prepare the library. Novagen company was used for sequencing using Illumine hiseq 2500 technology and paired-end reads. Several software such as hisat2, cufflinks, stringtie, cuffmerge and cuffdiff were used for mapping, aligning and analysis of gene expression differences. In order to extract coding and non-coding genes, FEELnc software was used with default settings. Potential target genes of lncRNAs were investigated by searching for protein coding genes located within 100 kb upstream and downstream of each lncRNA. In the following, a positive and negative correlation of 90% was obtained between two groups of coding and non-coding genes based on the degree of expression change. In order to investigate the metabolic, structural and functional pathways of significant genes, the Enrichr database, which is connected with other databases such as KEGG, was used.
Results and Discussion:In the current research, a total of eight samples produced 187640642 million paired reads with a size of 150 nucleotides and after quality control, 185258819 uncontaminated reads were obtained. The number of 1421 lncRNA transcripts related to 921 gene loci and 154 related target genes were identified in the comparison between ascites and healthy birds. Then, this number of genes were identified (154 genes) in order to check their functional characteristics using the Enrichr database, five functional pathways Glycine, serine and threonine metabolism, Rap1 signaling pathway, Sphingolipid metabolism, Phosphatidylinositolsignaling system, Mucin type O-glycan biosynthesis and related genes were significant. Out of 13 significant lncRNAs in these biological pathways, 12 are located on the antisense direction and one is located on the sense direction. In addition, 9 lncRNAs are exonic, 3 intronic and 1 in downstream position. These pathways are activated as damage modifiers in hypoxic conditions caused by ascites and provide the required energy and maintain kidney homeostasis in response to oxygen tension caused by ascites. On the other hand, they act as cell survival, increase proliferation and anti-apoptosis, which on the one hand reduce kidney damage and on the other hand make it function better, and in this way, reduce complications caused by ascites kidney damage.
Conclusion: Therefore, by targeting the important pathways of biology obtained and the genes affecting them for the prevention and treatment of ascites disease, it will provide a new insight for breeding.

Keywords

Ascites; Broiler; Kidney; lncRNA; RNA-seq

References

1. Ablimit, T., Tursun, G., Zhang, Y., Abduxkur, G., Abdurexit, G., & Abliz, G. (2022). Inositol monophosphatase 2 promotes epithelial ovarian cancer cell proliferation and migration by regulating the AKT/mTOR signaling pathway. Experimental and Therapeutic Medicine, 24(5), 1-8.
2. Adetula, A. A., Gu, L., Nwafor, C. C., Du, X., Zhao, S., & Li, S. (2018). Transcriptome sequencing reveals key potential long non-coding RNAs related to duration of fertility trait in the uterovaginal junction of egg-laying hens. Scientific Reports, 8(1), 13185.
3. Ali, H., Abu-Farha, M., Hammad, M. M., Devarajan, S., Bahbahani, Y., Al-Khairi, I., & Al-Mulla, F. (2022). Potential role of N-Cadherin in diagnosis and prognosis of diabetic nephropathy. Frontiers in Endocrinology, 13, 882700.
4. Alikhan, M. A., Jones, C. V., Williams, T. M., Beckhouse, A. G., Fletcher, A. L., Kett, M. M., & Deane, J. A. (2011). Colony-stimulating factor-1 promotes kidney growth and repair via alteration of macrophage responses. The American Journal of Pathology, 179(3), 1243-1256.
5. Arai, R., Ito, K., Ohnishi, T., Ohba, H., Akasaka, R., Bessho, Y., & Yokoyama, S. (2007). Crystal structure of human myo-inositol monophosphatase 2, the product of the putative susceptibility gene for bipolar disorder, schizophrenia, and febrile seizures. Proteins: Structure, Function, and Bioinformatics, 67(3), 732-742.
6. Balla, T., Szentpetery, Z., & Kim, Y. J. (2009). Phosphoinositide signaling: new tools and insights. Physiology. 24, 231–244.. doi: 10.1152/physiol.00014.2009.
7. Balzac, F., Avolio, M., Degani, S., Kaverina, I., Torti, M., Silengo, L., & Retta, S. F. (2005). E-cadherin endocytosis regulates the activity of Rap1: a traffic light GTPase at the crossroads between cadherin and integrin function. Journal of Cell Science, 118(20), 4765-4783.
8. Bergstrom, K. S., & Xia, L. (2013). Mucin-type O-glycans and their roles in intestinal homeostasis. Glycobiology, 23(9), 1026-1037.
9. Chinwalla, A. T., Cook, L. L., Delehaunty, K. D., Fewell, G. A., Fulton, L. A., Fulton, R. S., & Members of the Mouse GenomeAnalysis, G. (2002). Initial sequencing and comparative analysis of the mouse genome. Nature, 420(6915), 520-562. http://dx.doi.org/10.1038/nature01262
10. Cowen, B., Rothenbacher, H., Schwartz, L., Braune, M., & Owen, R. (1988). A case of acute pulmonary edema, splenomegaly, and ascites in Guinea fowl. Avian Diseases, 32(1), 151-156.
11. Docherty, N. G., Calvo, I. F., Quinlan, M. R., Pérez-Barriocanal, F., McGuire, B. B., Fitzpatrick, J. M., & Watson, R. W. G. (2009). Increased E-cadherin expression in the ligated kidney followingunilateral ureteric obstruction. Kidney International, 75(2), 205-213.
12. Gao, L., Liu, M. M., Zang, H. M., Ma, Q. Y., Yang, Q., Jiang, L., & Wang, J. N. (2018). Restoration of E-cadherin by PPBICA protects against cisplatin-induced acute kidney injuryby attenuating inflammation and programmed cell death. Laboratory Investigation, 98(7), 911-923.
13. Guo, D., Zhang, J., Han, Y., Cui, L., Wang, H., Wang, K., & Duan, Z. (2023). Transcriptomic study on the lungs of broilers with ascites syndrome. Animals, 13(1), 175.
14. Gupta, A. (2011). Ascites syndrome in poultry: A review. World's Poultry Science Journal, 67(3), 457-468.
15. Hasanpur, K., Nassiri, M., & Hosseini Salekdeh, G. (2019). The comparative analysis of phenotypic and whole transcriptome gene expression data of ascites susceptible versus ascites resistant chickens. Molecular Biology Reports, 46, 793-804.
16. Hayashi, D., Yagi, K., Song, C., Ueda, S., Yamanoue, M., Topham, M., & Shirai, Y. (2017). Diacylglycerol kinase alpha is involved in the vitamin E-induced amelioration of diabetic nephropathy in mice. Scientific Reports, 7(1), 2597.
17. Honda, T., Hirakawa, Y., & Nangaku, M. (2019). The role of oxidative stress and hypoxia in renal disease. Kidney Research and Clinical Practice, 38(4), 414.
18. Hu, , Chen, S., Jia, C., Xue, S., Dou, C., Dai, Z., & Cui, H. (2018). Gene expression profile and long non-coding RNA analysis, using RNA-Seq, in chicken embryonic fibroblast cells infected by avian leukosis virus J. Archives of Virology, 163, 639-647.
19. Jin, J., Hou, Q., Mullen, T. D., Zeidan, Y. H., Bielawski, J., Kraveka, J. M., & Hsu, Y. T. (2008). Ceramide generated by sphingomyelin hydrolysis and the salvage pathway is involved in hypoxia/reoxygenation-induced Bax redistribution to mitochondriain NT-2 cells. Journal of Biological Chemistry, 283(39), 26509-26517.
20. Kiryluk, K., Li, Y., Moldoveanu, Z., Suzuki, H., Reily, C., Hou, P., & Fischman, C. (2017). GWAS for serum galactose-deficient IgA1 implicates critical genes of the O-glycosylation pathway. PLoS Genetics, 13(2), e1006609.
21. Kosinska-Selbi, B., Mielczarek, M., & Szyda, J. (2020). Long non-coding RNA in livestock. Animal, 14(10), 2003-2013.
22. Kunrath-Lima, M., de Miranda, M. C., da Fonseca Ferreira, A., Faraco, C. C. F., de Melo, M. I. A., Goes, A. M., & Gomes, D. A. (2018). Phospholipase C delta 4 (PLCδ4) is a nuclear protein involved in cell proliferation and senescence in mesenchymal stromalstem cells. Cellular Signalling, 49, 59-67.
23. Lee, K. P., Anthony, N. B., Orlowski, S. K., & Rhoads, D. D. (2022). SNP-based breeding for broiler resistance to ascites and evaluation of correlated production traits. Hereditas, 159(1), 1-15.
24. Levy, M., & Futerman, A. H. (2010). Mammalian ceramide synthases. IUBMB Life, 62(5), 347-356.
25. Li, D., Li, F., Jiang, K., Zhang, M., Han, R., Jiang, R., & Kang, X. (2019). Integrative analysis of long noncoding RNA and mRNA reveals candidate lncRNAs responsible formeat quality at different physiological stages in Gushi chicken. PloS One, 14(4), e0215006.
26. Li, G. S., Zhang, H., Lv, J. C., Shen, Y., & Wang, H. Y. (2007). Variants of C1GALT1 gene are associated with the genetic susceptibility to IgA nephropathy. Kidney International, 71(5), 448-453.
27. Li, M., Xiao, D., Zhang, J., Qu, H., Yang, Y., Yan, Y., & Wang, J. (2016). Expression of LPA2 is associated with poor prognosis in human breast cancer and regulates HIF-1α expression and breast cancer cell growth. Oncology Reports, 36(6), 3479-3487.
28. Lin, Y. F., Chou, J. L., Chang, J. S., Chiu, I. J., Chiu, H. W., & Lin, Y. F. (2019). Dysregulation of the miR-25-IMPA2 axis promotes metastatic progression in clear cell renal cell carcinoma. EBioMedicine, 45, 220-230.
29. Liu, Y., Sun, Y., Li, Y., Bai, H., Xue, F., Xu, S., & Chen, J. (2017). Analyses of long non-coding RNA and mRNA profiling using RNA sequencing in chicken testis with extreme sperm motility. Scientific Reports, 7(1), 1-8.
30. Lorenzen, J. M., Haller, H., & Thum, T. (2011). MicroRNAs as mediators and therapeutic targets in chronic kidney disease. Nature Reviews Nephrology, 7(5(, 286–294. http://dx.doi.org/ 10.1038/nrneph.2011.26
31. Lorenzen, J. M., & Thum, T. (2016). Long noncoding RNAs in kidney and cardiovascular diseases. Nature Reviews Nephrology, 12(6), 360-373.
32. Malekshahdehi, S., Hafezian, S., Rahimi-Mianji, G., & Hasanpur, K. (2021). Investigation of gender differences in the incidence of ascites and profile of gene expression in kidney tissue of broiler chickens. Animal Production Research, 10(3), 33-44.
33. Marciano, D. K., Brakeman, P. R., Lee, C.-Z., Spivak, N., Eastburn, D. J., Bryant, M., & Reichardt, L. F. (2011). p120 catenin is required for normal renal tubulogenesis and glomerulogenesis. Development, 138(10), 2099-2109.
34. Menke, J., Iwata, Y., Rabacal, W. A., Basu, R., Yeung, Y. G., Humphreys, B. D., & Kelley, V. R. (2009). CSF-1 signals directly to renal tubular epithelial cells to mediate repair in mice. The Journal of Clinical Investigation, 119(8), 2330-2342.
35. Nagano, T., Yamao, S., Terachi, A., Yarimizu, H., Itoh, H., Katasho, R., & Kikkawa, U. (2019). D-aminoacid oxidase promotes cellular senescence via the production of reactive oxygen species. Life Science Alliance, 2(1), 1-14.
36. Nemati, M., Shahir, M., Harakinezhad, M., & Lotfalhian, H. (2017). Cold-induced ascites in broilers: effects of vitamin C and coenzyme Q10. Brazilian Journal of Poultry Science, 19, 537-544.
37. Ning, B., Guo, C., Kong, A., Li, K., Xie, Y., Shi, H., & Gu, J. (2021). Calcium signaling mediates cell death and crosstalk with autophagy in kidney disease. Cells, 10(11), 3204.
38. Ohnishi, T., Ohba, , Seo, K. C., Im, J., Sato, Y., Iwayama, Y., & Yoshikawa, T. (2007). Spatial expression patterns and biochemical properties distinguish a second myo-inositol monophosphatase IMPA2 from IMPA1. Journal of Biological Chemistry, 282(1), 637-646.
39. Ohnishi, T., Tanizawa, Y., Watanabe, A., Nakamura, T., Ohba, H., Hirata, H., & Watanabe, K. (2013). Human myo-inositol monophosphatase 2 rescues the nematode thermotaxis mutant ttx-7 more efficiently than IMPA 1: Functional and evolutionary considerations of the two mammalian myo-inositol monophosphatase genes. Journal of Neurochemistry, 124(5), 685-694.
40. Ørom, U. A., Derrien, T., Beringer, M., Gumireddy, K., Gardini, A., Bussotti, G., & Shiekhattar, R. (2010). Long noncoding RNAs with enhancer-like function in human cells. Cell, 143(1), 46-58. http://dx.doi.org/10.1016/j.cell.2010.09.001
41. Peng, Y., Chang, L., Wang, Y., Wang, R., Hu, L., Zhao, Z., & Li, J. (2019). Genome-wide differential expression of long noncoding RNAs and mRNAs in ovarian follicles of two different chicken breeds. Genomics, 111(6), 1395-1403.
42. Ravidà, A., Musante, L., Kreivi, M., Miinalainen, I., Byrne, B., Saraswat, M., & Holthofer, H. (2015). Glycosylation patterns of kidney proteins differ in rat diabetic nephropathy. Kidney International, 87(5), 963-974.
43. Rebecchi, M. J., & Pentyala, S. N. (2000). Structure, function, and control of phosphoinositide-specific phospholipase C. Physiological Reviews, 80(4), 1291-1335.
44. Reddy, M. A., & Natarajan, R. (2021). Cooperative activation of divergent pathways by LPAR1 and LPAR2 receptors in fibrotic signaling. American Journal of Physiology-Renal Physiology, 320(3), F322-f324. http://dx.doi.org/10.1152/ajprenal.00685.2020
45. Ren, T., Li, Z., Zhou, Y., Liu, X., Han, R., Wang, Y., & Kang, X. (2018). Sequencing and characterization of lncRNAs in the breast muscle of Gushi and Arbor Acres chickens. Genome, 61(5), 337-347.
46. Ronco, C., McCullough, P., Anker, S. D., Anand, I., Aspromonte, N., Bagshaw, S. M., Bellomo, R., Berl, T., Bobek, I., & Cruz, D. N, (2010). Cardio-renal syndromes: Report from the consensus conference of the acute dialysis quality initiative. European Heart Journal, 31(6), 703-711.
47. Sakane, F., Hoshino, F., Ebina, M., Sakai, H., & Takahashi, D. (2021). The roles of diacylglycerol kinase α in cancer cell proliferation and apoptosis. Cancers, 13(20), 1-13.
48. Shi, S., Shen, Y., Zhang, S., Zhao, Z., Hou, Z., Zhou, H., & Guo, Y. (2017). Combinatory evaluation of transcriptome and metabolome profiles of low temperature-induced resistant ascites syndrome in broiler chickens. Scientific Reports, 7(1), 1-16.
49. Song, K., Fu, J., Song, J., Herzog, B. H., Bergstrom, K., Kondo, Y., & Lupu, F. (2017). Loss of mucin-type O-glycans impairs the integrity of the glomerular filtration barrier in the mouse kidney. Journal of Biological Chemistry, 292(40), 16491–16497.
50. Stotter, B. R., Talbot, B. E., Capen, D. E., Artelt, N., Zeng, J., Matsumoto, Y., & Schlondorff, J. S. (2020). Cosmc-dependent mucin-type O-linked glycosylation is essential for podocyte function. American Journal of Physiology-Renal Physiology, 318(2), F518-F530.
51. Suzuki, R., Nakamura, Y., Koiwai, R., Fuseya, S., Murakami, Y., Hagiwara, K., & Kudo, T. (2022). global loss of core 1-derived o-glycans in mice leads to high mortality due to acute kidney failure and gastric ulcers. International Journal of Molecular Sciences, 23(3), 1273.
52. Taghizadeh, V., Nassiri, M.R., Tahmoorespur, M., Bakhtiarizadeh, M. R., & Javadmanesh, A. (2018). Gene expression network analysis on angiogenesis pathway in low temperature-induced ascites susceptible chickens in B-line pedigree of Iranian meat-type strain, Arian. Iranian Journal of Animal Science Research, 10(2), 249-262. In Persian with English Summary.
53. Wandall, H. H., Nielsen, M. A., King-Smith, S., de Haan, N., & Bagdonaite, I. (2021). Global functions of O-glycosylation: promises and challenges in O-glycobiology. The FEBS Journal, 288(24), 7183-7212.
54. Xiao, Y., Hu, J., & Yin, W. (2018). Systematic identification of non-coding RNAs. Non-coding RNAs in Complex Diseases: A Bioinformatics Perspective, 9-18.
55. Xie, L. S., Qin, W., Fan, J. M., Huang, J., Xie, X. S., & Li, Z. (2010). The role of C1GALT1C1 in lipopolysaccharide-induced IgA1 aberrant O-glycosylation in IgA nephropathy. Clinical and Investigative Medicine, E5-E13.
56. Yin, Z., Lian, L., Zhu, F., Zhang, Z. H., Hincke, M., Yang, N., & Hou, Z. C. (2020). The transcriptome landscapes of ovary and three oviduct segments during chicken (Gallus gallus) egg formation. Genomics, 112(1), 243-251. http://dx.doi.org/10.1016/j.ygeno.2019.02.003
57. Yokota, R., Bhunu, B., Toba, H., & Intapad, S. (2021). Sphingolipids and kidney disease: possible role of preeclampsia and intrauterinegrowth restriction (IUGR). Kidney360, 2(3), 534.
58. Yu, A., Zhao, J., Zhong, J., Wang, J., Yadav, S. P. S., Molitoris, B. A., & Mechref, Y. (2021). Altered O-glycomes of renal brush-border membrane in model rats with chronic kidney diseases. Biomolecules, 11(11), 1560.
59. Zhang, M. Z, Yao, B., Yang, S., Jiang, L., Wang, S., Fan, X., & Chen, J. (2012a). CSF-1 signaling mediates recovery from acute kidney injury. The Journal of Clinical Investigation, 122(12), 4519-4532.
60. Zhang, T., Zhang, X., Han, K., Zhang, G., Wang, J., Xie, K., & Fan, X. (2017). Analysis of long noncoding RNA and mRNA using RNA sequencing during the differentiation of intramuscular preadipocytes in chicken. PloS One, 12(2), e0172389.
61. Zhang , X. (2021). A Brief Note on Phosphatidylinositol (PI) Signal Pathway. Journal of Cell Signaling, 6(11), 1.
62. Zhang, Yi. L., Wang, R. C., Cheng, K., Ring, B. Z., & Su, L. (2017). Roles of Rap1 signaling in tumor cell migration and invasion. Cancer Biology & Medicine, 14(1), 90.
63. Zhang, Y., Baker, S. S., Baker, R. D., Zhu, R., & Zhu, L. (2012). Systematic analysis of the gene expression in the livers of nonalcoholic steatohepatitis: Implications on potential biomarkers and molecular pathological mechanism. PloS One, 7(12), e51131.

Zhang, Y., Su, W., Zhang, B., Ling, Y., Kim, W. K., & Zhang, H. (2021). Comprehensive analysis of coding and non-coding RNA transcriptomes related to hypoxic adaptation in Tibetan chickens. Journal of Animal Science and Biotechnology, 12, 1-14.