Redox disequilibrium vis-a-vis inflammatory cascade mediation of lymphocyte dysfunction, apoptosis, cytokine expression and activation of NF-κB in subclinical diabetic goats


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Authors

  • M I YATOO Assistant Professor, ICAR-Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh 243 122 India
  • U DIMRI Head, ICAR-Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh 243 122 India
  • M MASHOOQ PhD Scholar, ICAR-Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh 243 122 India
  • A SAXENA Senior Research Fellow, ICAR-Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh 243 122 India
  • A GOPALAKRISHNAN Assistant Professor, ICAR-Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh 243 122 India
  • S T BASHIR Post Graduate Student, University of Illinois, Urbana-Champaign, United States

https://doi.org/10.56093/ijans.v89i1.86378

Keywords:

Diabetes, Goat, Immunity, NF-κB, Oxidative stress

Abstract

Molecular basis of diabetes induced oxidative stress and immune dysfunction have not been reported in animal science. The present study envisages same in subclinical diabetic (SCD) goats (6) diagnosed on biochemical and histopathological basis in reference to non-diabetic (NSCD) goats (6). Oxidative stress indices were analyzed by manual methods. The concentration of reduced glutathione (GSH) and the activity of superoxide dismutase (SOD) was significantly lower in SCD goats than in NSCD goats; whereas the lipid peroxide (LPO) was higher in SCD. Catalase (CAT) activity was nonsignificantly lower in SCD goats than NSCD goats. SCD goats had significantly lower lymphocyte stimulation index by cell culture and higher apoptotic cell percentage by flow cytometry than NSCD goats. The concentration of the transforming growth factor beta 1 (TGF-β1) by ELISA was significantly higher in SCD goats than in NSCD. The expressions of tumour necrosis factor alpha (TNF-α) and interleukin 8 (IL 8) by RT-PCR were higher in SCD goats than in non-diabetic ones. Expression of transcription factor (NF-κB) by western blot was significantly higher in SCD goats than NSCD goats. Fall of antioxidants (GSH, SOD, catalase) and rise of oxidants (LPO) suggest oxidative stress. Decrease of immune cell function, rise of inflammatory cytokines and transcription factors suggest immune dysfunction. Hence it was concluded that SCD induced oxidative stress and impairment of immunity in goats, which was most likely associated with depletion of antioxidants, increase of oxidants and inflammatory mediators. NF-κB, most likely have played a mediatory role in coordinating these intricate responses.

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References

ADA. 2018. Diagnosis and classification of diabetes mellitus. American Diabetes Association. Diabetes Care 35: 64–71. DOI: https://doi.org/10.2337/dc12-s064

Alayash A I, El-Hassan A M, Omer R and Bonaventura J. 1988. Glycosylated haemoglobin: an indicator of long-term blood glucose in domestic sheep and goats. Comparative Biochemistry Physiology A: Comparative Physiology 90: 229– 31.

Al-Qudah K M. 2011. Oxidant and antioxidant profile of hyperketonemic ewes affected by pregnancy toxemia. Veterinary Clinical Pathology 40: 60–65.

Bergmeyer H U. 1983. UV method of catalase assay. Methods of Enzymatic Analysis. 3rd edn. (Ed.) Bansal S K. Weinheim. Deer Field Beach, Florida, pp 273.

Bernabucci U, Ronchi B, Lacetera N and Nardone A. 2005. Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows. Journal of Dairy Science 88: 2017–26.

Braun U, Gansohr B and Seidel M. 2008. Diabetes mellitus type 1 in a goat. Schweiz Archives Tierheilkd 150: 608–12.

Celi P, Trana A D and Claps S. 2008. Effects of perinatal nutrition on lactational performance, metabolic and hormonal profiles of dairy goats and respective kids. Small Ruminant Research 79: 129–36.

Ceriello A. 1998. The emerging role of post-prandial hyperglycemic spikes in the pathogenesis of diabetic complications. Diabetes 15: 188–93.

Chomczynski P and Sacchi N. 1987. Single-step method of RNA isolation by acid guanidiniumthiocyanate–phenol–chloroform extraction. Annals Biochemistry 162: 156–59.

Clark Z. 2003. Diabetes mellitus in a 6-month-old Charolais. Canadian Veterinary Journal 44: 921–922.

Dar P A, Hajam I A, Suryanarayan V S, Kishore S and Kondabattul G. 2015. Kinetics of cytokine expression in bovine PBMCs and whole blood after in vitro stimulation with foot-and-mouth disease virus (FMDV) antigen. Cytokine 72: 58–62.

de Arriba S G, Loske C, Meiners I, Fleischer G, Lobisch M, Wessel K, Tritschler H, Schinzel R and Münch G. 2003. Advanced glycation end products induce changes in glucose consumption, lactate production, and ATP levels in SH-SY5Y neuroblastoma cells by a redox-sensitive mechanism. Journal Cerebral Blood Flow Metabolism 23: 1307–13.

de Carvalho V F, Guedes C P, Gonçalves P L and de Cássia G A R. 2012. The role of hyperglycemia in the induction of oxidative stress and inflammatory process. Nutricion Hospitalaria 27: 1391–98.

Deepa P M, Dimri U, Jhambh R, Yatoo M I and Sharma B. 2015. Alteration in clinico-biochemical profile and oxidative stress indices associated with hyperglycaemia with special reference to diabetes in cattle-a pilot study. Tropical Animal HealthADA. 2018. Diagnosis and classification of diabetes mellitus. American Diabetes Association. Diabetes Care 35: 64–71.

Alayash A I, El-Hassan A M, Omer R and Bonaventura J. 1988. Glycosylated haemoglobin: an indicator of long-term blood glucose in domestic sheep and goats. Comparative Biochemistry Physiology A: Comparative Physiology 90: 229– 31. DOI: https://doi.org/10.1016/0300-9629(88)91108-5

Al-Qudah K M. 2011. Oxidant and antioxidant profile of hyperketonemic ewes affected by pregnancy toxemia. Veterinary Clinical Pathology 40: 60–65. DOI: https://doi.org/10.1111/j.1939-165X.2011.00284.x

Bergmeyer H U. 1983. UV method of catalase assay. Methods of Enzymatic Analysis. 3rd edn. (Ed.) Bansal S K. Weinheim. Deer Field Beach, Florida, pp 273.

Bernabucci U, Ronchi B, Lacetera N and Nardone A. 2005. Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows. Journal of Dairy Science 88: 2017–26. DOI: https://doi.org/10.3168/jds.S0022-0302(05)72878-2

Braun U, Gansohr B and Seidel M. 2008. Diabetes mellitus type 1 in a goat. Schweiz Archives Tierheilkd 150: 608–12. DOI: https://doi.org/10.1024/0036-7281.150.12.608

Celi P, Trana A D and Claps S. 2008. Effects of perinatal nutrition on lactational performance, metabolic and hormonal profiles of dairy goats and respective kids. Small Ruminant Research 79: 129–36. DOI: https://doi.org/10.1016/j.smallrumres.2008.07.010

Ceriello A. 1998. The emerging role of post-prandial hyperglycemic spikes in the pathogenesis of diabetic complications. Diabetes 15: 188–93. DOI: https://doi.org/10.1002/(SICI)1096-9136(199803)15:3<188::AID-DIA545>3.0.CO;2-V

Chomczynski P and Sacchi N. 1987. Single-step method of RNA isolation by acid guanidiniumthiocyanate–phenol–chloroform extraction. Annals Biochemistry 162: 156–59. DOI: https://doi.org/10.1016/0003-2697(87)90021-2

Clark Z. 2003. Diabetes mellitus in a 6-month-old Charolais. Canadian Veterinary Journal 44: 921–922.

Dar P A, Hajam I A, Suryanarayan V S, Kishore S and Kondabattul G. 2015. Kinetics of cytokine expression in bovine PBMCs and whole blood after in vitro stimulation with foot-and-mouth disease virus (FMDV) antigen. Cytokine 72: 58–62. DOI: https://doi.org/10.1016/j.cyto.2014.12.011

de Arriba S G, Loske C, Meiners I, Fleischer G, Lobisch M, Wessel K, Tritschler H, Schinzel R and Münch G. 2003. Advanced glycation end products induce changes in glucose consumption, lactate production, and ATP levels in SH-SY5Y neuroblastoma cells by a redox-sensitive mechanism. Journal Cerebral Blood Flow Metabolism 23: 1307–13. DOI: https://doi.org/10.1097/01.WCB.0000090622.86921.0E

de Carvalho V F, Guedes C P, Gonçalves P L and de Cássia G A R. 2012. The role of hyperglycemia in the induction of oxidative stress and inflammatory process. Nutricion Hospitalaria 27: 1391–98.

Deepa P M, Dimri U, Jhambh R, Yatoo M I and Sharma B. 2015. Alteration in clinico-biochemical profile and oxidative stress indices associated with hyperglycaemia with special reference to diabetes in cattle-a pilot study. Tropical Animal Health diabetes mellitus in a goat. Journal Faculty Veterinary Medicine University Istanbul 27: 7–12.

Liu H, Cao M M, Wang Y, Li L C, Zhu L B, Xie G Y and Li Y B. 2015. Endoplasmic reticulum stress is involved in the connection between inflammation and autophagy in type 2 diabetes. General Comparative Endocrinology 210: 124–29. DOI: https://doi.org/10.1016/j.ygcen.2014.09.006

Livak K J and Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402–08. DOI: https://doi.org/10.1006/meth.2001.1262

Lowry O H, Rosebrough N J, Farr A L and Randall R J. 1951. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193: 265–75. DOI: https://doi.org/10.1016/S0021-9258(19)52451-6

Luo B, Chan W F, Lord S J, Nanji S A, Rajotte R V, Shapiro A M and Anderson C C. 2007. Diabetes induces rapid suppression of adaptive immunity followed by homeostatic T-cell proliferation. Scandinavian Journal of Immunology 65: 22– 31. DOI: https://doi.org/10.1111/j.1365-3083.2006.01863.x

Madesh M and Balasubramanian K A. 1998. Microtitre plate assay for superoxide dismutase using MTT reduction by superoxide. Indian Journal of Biochemistry and Biophysics 35: 184–188.

Meier H. 1960. Diabetes mellitus in animals: a review. Diabetes 9: 485–89. DOI: https://doi.org/10.2337/diab.9.6.485

Morohoshi M, Fujisawa K, Uchimura I and Numano F. 1996. Glucose-dependent interleukin 6 and tumour necrosis factor production by human peripheral blood monocytes in vitro. Diabetes 45: 954–59. DOI: https://doi.org/10.2337/diabetes.45.7.954

Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. Journal of Immunological Methods 65: 55–63. DOI: https://doi.org/10.1016/0022-1759(83)90303-4

Mozzini C, Garbin U, Stranieri C, Pasini A, Solani E, Tinelli I A, Cominacini L and Fratta Pasini A M. 2015. Endoplasmic reticulum stress and Nrf2 repression in circulating cells of type 2 diabetic patients without the recommended glycemic goals. Free Radical Research 49: 244–52. DOI: https://doi.org/10.3109/10715762.2014.997229

Mytilineou C, Kramer B C and Yabut J A. 2002. Glutathione depletion and oxidative stress. Parkinsonism Related Disorders 8: 385–87. DOI: https://doi.org/10.1016/S1353-8020(02)00018-4

Nowotny K, Jung T, Höhn A, Weber D and Grune T. 2015. Advanced glycation end products and oxidative stress in type 2 diabetes mellitus. Biomolecules 5: 194–222. DOI: https://doi.org/10.3390/biom5010194

Pertyñska-Marczewska M, Kiriakidis S, Wait R, Beech J, Feldmann M and Paleolog E M. 2004. Advanced glycation end products upregulate angiogenic and pro-inflammatory cytokine production in human monocyte/macrophages. Cytokine 28: 35–47. DOI: https://doi.org/10.1016/j.cyto.2004.06.006

Pickering R J, Rosado C J, Sharma A, Buksh S, Tate M and de Haan J B. 2018. Recent novel approaches to limit oxidative stress and inflammation in diabetic complications. Clin Transl Immunology 7: e1016. DOI: https://doi.org/10.1002/cti2.1016

Placer Z A, Cushman L L and Johnson B. 1966. Estimation of product of lipid peroxidation (malonaldehyde) in biochemical system. Annals Biochemistry 16: 359–64. DOI: https://doi.org/10.1016/0003-2697(66)90167-9

Prins H K and Loos J A. 1969. Biochemical Methods in Red Cell Genetics. Academic Press, London, UK. pp 530.

Radostits O M, Gay C C, Blood D C and Hinchcliff K W. 2000. Veterinary Medicine—A Textbook for the Diseases of Cattle, Sheep, Pigs, Goats and Horses. 9th edn. W B Saunders, London, pp 1819–22.

Reis J P, Allen N B, Bancks M P, Carr J J, Lewis C E, Lima J A, Rana J S, Gidding S S and Schreiner P J. 2018. Duration of diabetes and prediabetes during adulthood and subclinical atherosclerosis and cardiac dysfunction in middle age: The CARIA study. Diabetes Care 41: 731–38. DOI: https://doi.org/10.2337/dc17-2233

Saxena A, Yadav D, Maurya A K, Kumar A, Mohanty S, Gupta M M, Lingaraju M C, Yatoo M I, Thakur U S and Bawankule D U. 2015. Diarylheptanoids from Alnus nepalensis attenuates LPS-induced inflammation in macrophages and endotoxic shock in mice. International Immunopharmacology 8: 129– 36. DOI: https://doi.org/10.1016/j.intimp.2015.12.002

Schulze P C, Yoshioka J, Takahashi T, He Z, King G L and Lee R T. 2004. Hyperglycemia promotes oxidative stress through inhibition of thioredoxin function by thioredoxin-interacting protein. Journal of Biological Chemistry 279: 30369–374. DOI: https://doi.org/10.1074/jbc.M400549200

Shahbazkia H R and Nazifi S. 2008. Determination of glycated haemoglobin (HbG) and its correlation with plasma glucose in Iranian fat tailed sheep and lamb. Online Journal of Veterinary Research 12: 7–13.

Sharma A, Tate M, Mathew G, Vince J E, Ritchie R H and de Haan J B. 2018. Oxidative stress and NLRP3-Inflammasome activity as significant drivers of diabetic cardiovascular complications: therapeutic implications. Frontiers in Physiology 9: 114. DOI: https://doi.org/10.3389/fphys.2018.00114

Smoak I W. 2004. Hyperglycemia-induced TGFb and fibronectin expression in embryonic mouse heart. Development Dynamics 231: 179–89. DOI: https://doi.org/10.1002/dvdy.20123

Smulders Y and Serné E. 2018. Is HbA1c a good diagnostic test for (pre)diabetes in cardiac rehabilitation patients? European Journal of Preventive Cardiology 25: 462–63. DOI: https://doi.org/10.1177/2047487318757553

Stirban A, Gawlowski T and Roden M. 2013. Vascular effects of advanced glycation end products: Clinical effects and molecular mechanisms. Molecular Metabolism 3: 94–108. DOI: https://doi.org/10.1016/j.molmet.2013.11.006

Tajima M, Yuasa M, Kawanabe M, Taniyama H, Yamato O and Maede Y. 1999. Possible causes of diabetes mellitus in cattle infected with bovine viral diarrhoea virus. Journal of Veterinary Medicine 46: 207–15. DOI: https://doi.org/10.1046/j.1439-0450.1999.00230.x

Taniyama H, Shirakawa T, Uruoka H F, Osame S, Kitamura N and Miyazawa K. 1993. Spontaneous diabetes mellitus in young cattle: histologic, immunohistochemical, and electron microscopic studies of the islets of Langerhans. Veterinary Pathology 30: 46–54. DOI: https://doi.org/10.1177/030098589303000106

Tentori L and Salvati A M. 1981. Haemoglobinometry in human blood. Methods Enzymology 76: 707–15. DOI: https://doi.org/10.1016/0076-6879(81)76152-4

Todd S E, Oliver M H, Jaquiery A L, Bloomfield F H and Harding J E. 2009. Periconceptional undernutrition of ewes impairs glucose tolerance in their adult offspring. Pediatric Research 65: 409–13. DOI: https://doi.org/10.1203/PDR.0b013e3181975efa

Turina M, Fry D E and Polk H C Jr. 2005. Acute hyperglycemia and the innate immune system: clinical, cellular, and molecular aspects. Critical Care Medicine 33: 1624–33. DOI: https://doi.org/10.1097/01.CCM.0000170106.61978.D8

Van Oostveldt K, Vangroenweghe F, Dosogne H and Burvenich C. 2001. Apoptosis and necrosis of blood and milk polymorphonuclear leukocytes in early and mid lactating healthy cows. Veterinary Research 32: 617–22. DOI: https://doi.org/10.1051/vetres:2001143

Vidigal F C, Cocate P G, Pereira L G and Alfenas R C G. 2012. The role of hyperglycemia in the induction of oxidative stress and inflammatory process. Nutricion Hospitalaria 27: 1391– 98.

Volpe C M O, Villar-Delfino P H, Dos Anjos P M F and Nogueira- Machado J A. 2018. Cellular death, reactive oxygen species (ROS) and diabetic complications. Cell Death and Disease 9: 119. DOI: https://doi.org/10.1038/s41419-017-0135-z

Yatoo M I, Deepa P M, Mandal R S K, Sharma B, Mendiratta S K, Patel B H M and Dimri U. 2015. Prevalence of subclinical diabetes in a commercial flock of dairy goats in India and its interaction with milk quality. Small Ruminant Research 132: 1–11. DOI: https://doi.org/10.1016/j.smallrumres.2015.09.012

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2019-01-22

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2019-01-22

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YATOO, M. I., DIMRI, U., MASHOOQ, M., SAXENA, A., GOPALAKRISHNAN, A., & BASHIR, S. T. (2019). Redox disequilibrium vis-a-vis inflammatory cascade mediation of lymphocyte dysfunction, apoptosis, cytokine expression and activation of NF-κB in subclinical diabetic goats. The Indian Journal of Animal Sciences, 89(1), 40–45. https://doi.org/10.56093/ijans.v89i1.86378
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