Porcine salivary proteome analysis identifies potential early pregnancy-specific protein biomarkers

MONTI DAS; ANKAN DE; PARTHASARATHI BEHERA; MOHAMMAD AYUB ALI; PRASANT KUMAR SUBUDHI; GIRIN KALITA; ASHULI KHOZHIIO KAYINA; JAGAN MOHANARAO GALI

doi:10.56093/ijans.v93i2.119316

Authors

MONTI DAS Central Agricultural University, Selesih, Aizawl, Mizoram 796 014 India
ANKAN DE College of Veterinary Sciences and Animal Husbandry, R. K. Nagar, West Tripura, Tripura
PARTHASARATHI BEHERA Central Agricultural University, Selesih, Aizawl, Mizoram 796 014 India
MOHAMMAD AYUB ALI Central Agricultural University, Selesih, Aizawl, Mizoram 796 014 India
PRASANT KUMAR SUBUDHI Central Agricultural University, Selesih, Aizawl, Mizoram 796 014 India
GIRIN KALITA Central Agricultural University, Selesih, Aizawl, Mizoram 796 014 India
ASHULI KHOZHIIO KAYINA Central Agricultural University, Selesih, Aizawl, Mizoram 796 014 India
JAGAN MOHANARAO GALI Central Agricultural University, Selesih, Aizawl, Mizoram 796 014 India

https://doi.org/10.56093/ijans.v93i2.119316

Keywords:

Biomarkers, Differentially expressed proteins, Early pregnancy, Pig, Saliva

Abstract

Early diagnosis of pregnancy is of utmost importance to optimize profit in pig husbandry. Identifying candidate protein biomarkers for early diagnosis of pregnancy in a non-invasive sample such as saliva may produce a colossal
lead to accomplish the purpose. Therefore, in this study, comparative salivary proteome profile of day 12 of gestation, representing elongation of blastocysts stage and non-pregnant sows was explored by label-free quantitation (LFQ) based mass spectrometry approach to identify early pregnancy biomarkers. A total of 115 proteins were identified as differentially expressed proteins (DEPs) with significant difference between non-pregnant and early pregnancy groups. Among the DEPs, majority of the proteins (82 out of 115 DEPs) were found to be down-regulated in early pregnancy group (fold change >2) compared to non-pregnant control. Functional classification and pathway analysis of the DEPs revealed involvement of most of the proteins in integrin signalling pathways, blood coagulation, carbohydrate metabolism, oxidative stress response and regulation of protein folding. Few DEPs with higher fold change during early pregnancy such as thioredoxin, heat shock 70 kDa protein 1A, alpha 1-S haptoglobin, and glutathione S-transferase pi 1 may have potential as biomarkers for early pregnancy diagnosis in pigs based on their recognized role in different pregnancy related activities. Overall, our results provide a set of salivary proteins which can be used as potential biomarkers for early pregnancy diagnosis after large scale validation.

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References

Bazer F W. 2013. Pregnancy recognition signaling mechanisms in ruminants and pigs. Journal of Animal Science and Biotechnology 4(1): 23. DOI: https://doi.org/10.1186/2049-1891-4-23

Berkova N, Lemay A, Dresser D W, Fontaine J Y, Kerizit J and Goupil S. 2001. Haptoglobin is present in human endometrium and shows elevated levels in the decidua during pregnancy. Molecular Human Reproduction 7(8): 747–54. DOI: https://doi.org/10.1093/molehr/7.8.747

Chae J I, Kim J, Lee S G, Jeon Y J, Kim D W, Soh Y, Seo K S, Lee H K, Choi N-J, Ryu J, Kang S, Cho S-K, Lee D-S, Chung H M and Koo D-B. 2011. Proteomic analysis of pregnancy-related proteins from pig uterus endometrium during pregnancy. Proteome Science 9: 41. DOI: https://doi.org/10.1186/1477-5956-9-41

Chae J I, Kim J, Lee S G, Koh M W, Jeon Y-J, Kim D-W, Ko S M, Seo K S, Lee H K, Choi N-J, Cho S-K, Ryu J, Kang K, Lee D-S, Chung H-M and Koo D-B. 2012. Quantitative proteomic analysis of pregnancy-related proteins from peripheral blood mononuclear cells during pregnancy in pigs. Animal Reproduction Science 134(3-4): 164–76. DOI: https://doi.org/10.1016/j.anireprosci.2012.07.008

De A, Ali M A, Chutia T, Onteru S K, Behera P, Kalita G, Sudarshan Kumar S and Gali J M. 2019. Comparative serum proteome analysis reveals potential early pregnancy-specific protein biomarkers in pigs. Reproduction, Fertility and Development 31(3): 613–31. DOI: https://doi.org/10.1071/RD18227

Dey A K, Kuma, B, Singh A K, Ranjan P, Thiruvengadam R, Desiraju B K, Kshetrapal P, Wadhwa N, Bhatnagar S, Rashid F, Malakar D, Salunke D M, Maiti T K and GARBH-Ini Study Group. 2020. Salivary proteome signatures in the early and middle stages of human pregnancy with term birth outcome. Scientific Reports 10(1): 8022. DOI: https://doi.org/10.1038/s41598-020-64483-6

Di Trapani G, Perkins A and Clarke F. 1998. Production and secretion of thioredoxin from transformed human trophoblast cells. Molecular Human Reproduction 4(4): 369–75. DOI: https://doi.org/10.1093/molehr/4.4.369

Gleichmann W, Bachmann G W, Dengler H J and Dudeck J. 1973. Effects of hormonal contraceptives and pregnancy on serum protein pattern. European Journal of Clinical Pharmacology 5: 218–25. DOI: https://doi.org/10.1007/BF00567007

Gutiérrez A M, Martínez-Subiela S, Eckersall P D and Cerón J. 2009. C-reactive protein quantification in porcine saliva: A minimally invasive test for pig health monitoring. Veterinary Journal 181: 261–65. DOI: https://doi.org/10.1016/j.tvjl.2008.03.021

Gutierrez A M, Miller I, Hummel K, Nobauer K, Martinez- Subiela S, Razzazi-Fazeli E, Gemeiner M and Cerón J J. 2011. Proteomic analysis of porcine saliva. Veterinary Journal 187(3): 356–62. DOI: https://doi.org/10.1016/j.tvjl.2009.12.020

Jalali B M, Bogacki M, Dietrich M, Likszo P and Wasielak M. 2015. Proteomic analysis of porcine endometrial tissue during peri-implantation period reveals altered protein abundance. Journal of Proteomics 1(125): 76–88. DOI: https://doi.org/10.1016/j.jprot.2015.05.003

Jalali B M, Likszo P, Andronowska A and Skarzynski D J. 2018. Alterations in the distribution of actin and its binding proteins in the porcine endometrium during early pregnancy: Possible role in epithelial remodeling and embryo adhesion. Theriogenology 116: 17–27. DOI: https://doi.org/10.1016/j.theriogenology.2018.05.004

Jalali B M, Likszo P and Skarzynski D J. 2016. Proteomic and network analysis of pregnancy-induced changes in the porcine endometrium on day 12 of gestation. Molecular Reproduction and Development 83(9): 827–41. DOI: https://doi.org/10.1002/mrd.22733

Jin D I, Lee H R, Kim H R, Lee H J, Yoon J T and Park C S. 2005. Proteomics analysis of pregnancy-specific serum proteins in bovine. Reproduction, Fertility and Development 18(1-2): 183. DOI: https://doi.org/10.1071/RDv18n2Ab151

Knapen M F, Peters W H, Mulder T P, Merkus H M, Jansen J B and Steegers E A. 1999. Plasma glutathione S-transferase Pi 1-1 measurements in the study of hemolysis in hypertensive disorders of pregnancy. Hypertension in Pregnancy 18(2): 147–56. DOI: https://doi.org/10.3109/10641959909023074

Li M and Huang S J. 2009. Innate immunity, coagulation and placenta-related adverse pregnancy outcomes. Thrombosis Research 124(6): 656–62. DOI: https://doi.org/10.1016/j.thromres.2009.07.012

Østrup E, Bauersachs S, Blum H, Wolf E and Hyttel P. 2010. Differential endometrial gene expression in pregnant and nonpregnant sows. Biology of Reproduction 83(2): 277–85. DOI: https://doi.org/10.1095/biolreprod.109.082321

Prickett J R and Zimmerman J J. 2010. The development of oral fluid-based diagnostics and applications in veterinary medicine. Animal Health Research Reviews 11(2): 207–16. DOI: https://doi.org/10.1017/S1466252310000010

Ramirez A, Wang C, Prickett J R, Pogranichniy R, Yoon KJ, Main R, Johnson J K, Rademacher C, Hoogland M, Hoffmann P, Kurtz A, Kurtz E and Zimmerman J. 2012. Efficient surveillance of pig populations using oral fluids. Preventive Veterinary Medicine 104(3-4): 292–300. DOI: https://doi.org/10.1016/j.prevetmed.2011.11.008

Rawat P, Bathla S, Baithalu R, Yadav M L, Kumar S, Ali S A, Tiwari A, Lotfan M, Naru J, Jena M, Behere P, Balhara A K, Vashisth R, Singh I, Dang A, Kaushik J K, Mohanty T K and Mohanty A K. 2016. Identification of potential protein biomarkers for early detection of pregnancy in cow urine using 2D DIGE and label free quantitation. Clinical Proteomics 13: 15. DOI: https://doi.org/10.1186/s12014-016-9116-y

Shen J, Zhou C, Zhu S, Shi W, Hu M, Fu X, Wang C, Wang Y, Zhang Q and Yu Y. 2014. Comparative transcriptome analysis reveals early pregnancy-specific genes expressed in peripheral blood of pregnant sows. PLoS ONE 9(12): e114036. DOI: https://doi.org/10.1371/journal.pone.0114036

Willis E L, Kersey D C, Durrant B S and Kouba A J. 2011. The acute phase protein ceruloplasmin as a non-invasive marker of pseudopregnancy, pregnancy, and pregnancy loss in the giant panda. PLoS ONE 6(7): e21159. DOI: https://doi.org/10.1371/journal.pone.0021159

Xu X, Len J Y, Gao F, Zhao Z A, Deng W B and Liang X H. 2014. Differential expression and anti-oxidant function of glutathione peroxidase 3 in mouse uterus during decidualization. FEBS Letters 588(9): 1580–89. DOI: https://doi.org/10.1016/j.febslet.2014.02.043

Zhang A, Sun H, Wang P and Wang X. 2013. Salivary proteomics in biomedical research. Clinica Chimica Acta 415: 261–65. DOI: https://doi.org/10.1016/j.cca.2012.11.001

Zhao H, Sui L, Miao K, An L, Wang D, Hou Z, Wang R, Guo M, Wang Z, Xu J, Wu Z and Tian J. 2015. Comparative analysis between endometrial proteomes of pregnant and non-pregnant ewes during the peri-implantation period map for pig serum proteins as a prerequisite for diagnostic applications. Journal of Animal Science and Biotechnology 6(1): 18. DOI: https://doi.org/10.1186/s40104-015-0017-0