DOI QR코드

DOI QR Code

Effects of High-Protein Diet and/or Resveratrol Supplementation on the Immune Response of Irradiated Rats

  • Kim, Kyoung Ok (Division of Food and Nutritional Science & Life Systems, College of Human Ecology, Sookmyung Women's University) ;
  • Park, Hyunjin (ICAN Nutrition Education and Research) ;
  • Kim, Hyun-Sook (Division of Food and Nutritional Science & Life Systems, College of Human Ecology, Sookmyung Women's University)
  • Received : 2014.04.16
  • Accepted : 2014.08.27
  • Published : 2014.09.30

Abstract

We investigated the effects of a high-protein diet and resveratrol supplementation on immune cells changes induced by abdominal irradiation in rats. Female Wistar rats were divided into 5 groups: 1) control diet, 2) control diet with irradiation 3) 30% high-protein diet with irradiation, 4) normal diet with resveratrol supplementation and irradiation, and 5) 30% high-protein diet with resveratrol supplementation and irradiation. We measured blood protein and albumin concentrations, lipid profiles, white blood cell (WBC) counts, proinflammatory cytokine production, and splenocyte proliferation in rats that had been treated with a 17.5 Gy dose of radiation 30 days prior. A high-protein diet affected plasma total cholesterol and very low density lipoprotein-cholesterol levels, which were increased by the radiation treatment. In addition, the lymphocyte percentage and immunoglobulin M (IgM) concentration were increased, and the neutrophil percentage was decreased in rats fed a high-protein diet. Resveratrol supplementation decreased the triglyceride (TG) level, but increased the IgM concentration and splenocyte proliferation. Proinflammatory cytokine production was lower in rats fed a high-protein diet supplemented with resveratrol than in rats fed a control diet. The results of the present study indicate that high-protein diets, with or without resveratrol supplementation, might assist with recovery from radiation-induced inflammation by modulating immune cell percentages and cytokine production.

Keywords

References

  1. Baur JA, Sinclair DA. 2006. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5: 493-506. https://doi.org/10.1038/nrd2060
  2. Iuga C, Alvarez-Idaboy J, Russo N. 2012. Antioxidant activity of trans-resveratrol toward hydroxyl and hydroperoxyl radicals: a quantum chemical and computational kinetics study. J Org Chem 77: 3868-3877. https://doi.org/10.1021/jo3002134
  3. Fauconneau B, Waffo-Teguo P, Huguet F, Barrier L, Decendit A, Merillon JM. 1997. Comparative study of radical scavenger and antioxidant properties of phenolic compounds from Vitis vinifera cell cultures using in vitro tests. Life Sci 61: 2103-2110. https://doi.org/10.1016/S0024-3205(97)00883-7
  4. Athar M, Back JH, Tang X, Kim KH, Kopelovich L, Bickers DR, Kim AL. 2007. Resveratrol: A review of preclinical studies for human cancer prevention. Toxicol Appl Pharmacol 224: 274-283. https://doi.org/10.1016/j.taap.2006.12.025
  5. Lin KH, Hsiao G, Shih CM, Chou DS, Sheu JR. 2009. Mechanisms of resveratrol-induced platelet apoptosis. Cardiovasc Res 83: 575-585. https://doi.org/10.1093/cvr/cvp139
  6. Brito PM, Devillard R, Negre-Salvayre A, Almeida LM, Dinis TC, Salvayre R, Auge N. 2009. Resveratrol inhibits the mTOR mitogenic signaling evoked by oxidized LDL in smooth muscle cells. Atherosclerosis 205: 126-134. https://doi.org/10.1016/j.atherosclerosis.2008.11.011
  7. Ungvari Z, Orosz Z, Rivera A, Labinskyy N, Xiangmin Z, Olson S, Podlutsky A, Csiszar A. 2007. Resveratrol increases vascular oxidative stress resistance. Am J Physiol Heart Circ Physiol 292: H2417-H2424. https://doi.org/10.1152/ajpheart.01258.2006
  8. Xiao M, Whitnall MH. 2009. Pharmacological countermeasures for the acute radiation syndrome. Curr Mol Pharmacol 2: 122-133. https://doi.org/10.2174/1874467210902010122
  9. Bentzen SM. 2006. Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nat Rev Cancer 6: 702-713. https://doi.org/10.1038/nrc1950
  10. Ostrau C, Hulsenbeck J, Herzog M, Schad A, Torzewski M, Lackner KJ, Fritz G. 2009. Lovastatin attenuates ionizing radiation-induced normal tissue damage in vivo. Radiother Oncol 92: 492-499. https://doi.org/10.1016/j.radonc.2009.06.020
  11. Reits EA, Hodge JW, Herberts CA, Groothuis TA, Chakraborty M, Wansley EK, Camphausen K, Luiten RM, de Ru AH, Neijssen J, Griekspoor A, Mesman E, Verreck FA, Spits H, Schlom J, van Veelen P, Neefjes JJ. 2006. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med 203: 1259-1271. https://doi.org/10.1084/jem.20052494
  12. Lee YJ, Auh SL, Wang Y, Burnette B, Wang Y, Meng Y, Beckett M, Sharma R, Chin R, Tu T, Weichselbaum RR, Fu YX. 2009. Therapeutic effects of ablative radiation on local tumor require $CD8^+$ T cells: changing strategies for cancer treatment. Blood 114: 589-595. https://doi.org/10.1182/blood-2009-02-206870
  13. Shin SJ, Yamada K, Sugisawa A, Saito K, Miyajima T, Umegaki K. 2002. Enhanced oxidative damage induced by total body irradiation in mice fed a low protein diet. Int J Radiat Biol 78: 425-432. https://doi.org/10.1080/09553000110119375
  14. Shin SJ. 2003. High levels of apoptosis induced by total body irradiation in mice fed a low protein-low vitamin E diet. Food Chem Toxicol 41: 665-670. https://doi.org/10.1016/S0278-6915(02)00331-9
  15. Kim KO, Park H, Chun M, Kim HS. 2014. Immunomodulatory effects of high protein diet with resveratrol supplementation on radiation-induced acute phase inflammation in rats. J Med Food 17: 963-971. https://doi.org/10.1089/jmf.2013.2976
  16. Chun M, Kang S, Jin YM, Oh YT, Kil HJ, Ahn BO, Oh TY. 2001. Radiation-induced proctitis in rat and role of nitric oxide. J Korean Soc Ther Radiol Onco 19: 265-274.
  17. Gridley DS, Obenaus A, Bateman TA, Pecaut MJ. 2008. Long-term changes in rat hematopoietic and other physiological systems after high-energy iron ion irradiation. Int J Radiat Biol 84: 549-559. https://doi.org/10.1080/09553000802203614
  18. Maier SF, Goehler LE, Fleshner M, Watkins LR. 1998. The role of the vagus nerve in cytokine-to-brain communication. Ann NY Acad Sci 840: 289-300. https://doi.org/10.1111/j.1749-6632.1998.tb09569.x
  19. Roubenoff R, Grinspoon S, Skolnik PR, Tchetgen E, Abad L, Spiegelman D, Knox T, Gorbach S. 2002. Role of cytokines and testosterone in regulating lean body mass and resting energy expenditure in HIV-infected men. Am J Physiol Endocrinol Metab 283: E138-E145. https://doi.org/10.1152/ajpendo.00426.2001
  20. Richardson RA, Davidson HI. 2003. Nutritional demands in acute and chronic illness. Proc Nutr Soc 62: 777-781. https://doi.org/10.1079/PNS2003302
  21. Klement RJ, Kammerer U. 2011. Is there a role for carbohydrate restriction in the treatment and prevention of cancer? Nutr Metab 8: 75. https://doi.org/10.1186/1743-7075-8-75
  22. Vazquez I, Gomez-de-Segura IA, Grande AG, Escribano A, Gonzalez-Gancedo P, Gomez A, Diez R, De Miguel E. 1999. Protective effect of enriched diet plus growth hormone administration on radiation-induced intestinal injury and on its evolutionary pattern in the rat. Dig Dis Sci 44: 2350-2358. https://doi.org/10.1023/A:1026637611298
  23. El-Missiry MA, Fayed TA, El-Sawy MR, El-Sayed AA. 2007. Ameliorative effect of melatonin against gamma-irradiationinduced oxidative stress and tissue injury. Ecotoxicol Environ Saf 66: 278-286. https://doi.org/10.1016/j.ecoenv.2006.03.008
  24. Pote MS, Gandhi NM, Mishra KP. 2006. Antiatherogenic and radioprotective role of folic acid in whole body $\gamma$-irradiated mice. Mol Cell Biochem 292: 19-25. https://doi.org/10.1007/s11010-006-9135-5
  25. Freudenberg A, Petzke KJ, Klaus S. 2012. Comparison of high-protein diets and leucine supplementation in the prevention of metabolic syndrome and related disorders in mice. J Nutr Biochem 23: 1524-1530. https://doi.org/10.1016/j.jnutbio.2011.10.005
  26. Feurgard C, Boehler N, Ferezou J, Serougne C, Aigueperse J, Gourmelon P, Lutton C, Mathe D. 1999. Ionizing radiation alters hepatic cholesterol metabolism and plasma lipoproteins in Syrian hamster. Int J Radiat Biol 75: 757-766. https://doi.org/10.1080/095530099140104
  27. Borek C. 2004. Antioxidants and radiation therapy. J Nutr 134: 3207S-3209S.
  28. Pratheeshkumar P, Kuttan G. 2010. Protective role of Vernonia cinerea L. against gamma radiation-induced immunosupression and oxidative stress in mice. Hum Exp Toxicol 30: 1022-1038.
  29. Park EJ, Hwang IS, Song JY, Jee YH. 2011. Acidic polysaccharide of Panax ginseng as a defense against small intestinal damage by whole-body gamma irradiation of mice. Acta Histochem 113: 19-23. https://doi.org/10.1016/j.acthis.2009.07.003
  30. Park SJ, Ahn GN, Lee NH, Park JW, Jeon YJ, Jee YH. 2011. Phloroglucinol (PG) purified from Ecklonia cava attenuates radiation-induced apoptosis in blood lymphocytes and splenocytes. Food Chem Toxicol 49: 2236-2242. https://doi.org/10.1016/j.fct.2011.06.021
  31. Zhang H, Zhai Z, Wang Y, Zhang J, Wu H, Wang Y, Li C, Li D, Lu L, Wang X, Chang J, Hou Q, Ju Z, Zhou D, Meng A. 2013. Resveratrol ameliorates ionizing irradiation-induced long-term hematopoietic stem cell injury in mice. Free Radic Biol Med 54: 40-50. https://doi.org/10.1016/j.freeradbiomed.2012.10.530
  32. Johnston CJ, Williams JP, Okunieff P, Finkelstein JN. 2002. Radiation-induced pulmonary fibrosis: examination of chemokine and chemokine receptor families. Radiat Res 157: 256-265. https://doi.org/10.1667/0033-7587(2002)157[0256:RIPFEO]2.0.CO;2
  33. Hosoi Y, Miyachi H, Matsumoto Y, Enomoto A, Nakagawa K, Suzuki N, Ono T. 2001. Induction of interleukin-$1\beta$ and interleukin-6 mRNA by low doses of ionizing radiation in macrophages. Int J Cancer 96: 270-276. https://doi.org/10.1002/ijc.1030
  34. Kindt TJ, Osborne BA, Goldsby RA. 2006. Kuby immunology. 6th ed. W. H. Freeman & Company, New York, NY, USA. p. 304-307.
  35. Sjostedt S, Bezak E. 2010. Non-targeted effects of ionising radiation and radiotherapy. Australas Phys Eng Sci Med 33: 219-231. https://doi.org/10.1007/s13246-010-0030-8
  36. Shin SC, Lee KM, Kang YM, Kim K, Kim CS, Yang KH, Jin YW, Kim CS, Kim HS. 2010. Alteration of cytokine profiles in mice exposed to chronic low-dose ionizing radiation. Biochem Biophys Res Commun 397: 644-649. https://doi.org/10.1016/j.bbrc.2010.05.121
  37. Mebius RE, Kraal G. 2005. Structure and function of the spleen. Nat Rev Immunol 5: 606-616. https://doi.org/10.1038/nri1669
  38. Jung JH, Kang JI, Kim HS. 2012. Effect of quercetin on impaired immune function in mice exposed to irradiation. Nutr Res Pract 6: 301-307. https://doi.org/10.4162/nrp.2012.6.4.301
  39. Lee YR, Jung JH, Kim HS. 2011. Hesperidin partially restores impaired immune and nutritional function in irradiated mice. J Med Food 14: 475-482. https://doi.org/10.1089/jmf.2010.1269
  40. Cortes-Barberena E, Ceballos-Olvera I, Gonzalez-Marquez H, Ortiz-Muniz R. 2013. Moderate and severe malnutrition alters proliferation of spleen cells in rats. Cell Prolif 46: 164-171. https://doi.org/10.1111/cpr.12019
  41. Duan WJ, Liu FL, He RR, Yuan WL, Li YF, Tsoi B, Su WW, Yao XS, Kurihara H. 2013. Autophagy is involved in the effects of resveratrol on prevention of splenocyte apoptosis caused by oxidative stress in restrained mice. Mol Nutr Food Res 57: 1145-1157. https://doi.org/10.1002/mnfr.201200662

Cited by

  1. Resveratrol promotes recovery of immune function of immunosuppressive mice by activating JNK/NF-κB pathway in splenic lymphocytes vol.95, pp.6, 2017, https://doi.org/10.1139/cjpp-2016-0404
  2. Distinct metabolic effects of resveratrol on lipogenesis markers in mice adipose tissue treated with high-polyunsaturated fat and high-protein diets vol.153, 2016, https://doi.org/10.1016/j.lfs.2016.04.014
  3. Effect of Resveratrol Dry Suspension on Immune Function of Piglets vol.2018, pp.1741-4288, 2018, https://doi.org/10.1155/2018/5952707
  4. Sexual Dimorphism, Age, and Fat Mass Are Key Phenotypic Drivers of Proteomic Signatures vol.16, pp.11, 2014, https://doi.org/10.1021/acs.jproteome.7b00501
  5. Resveratrol ameliorates ionizing irradiation-induced long-term immunosuppression in mice vol.94, pp.1, 2018, https://doi.org/10.1080/09553002.2018.1408976
  6. Subchronic toxicity evaluation of leaves from rabbiteye blueberry (Vaccinium virgatum Aiton) in rats vol.6, pp.None, 2014, https://doi.org/10.1016/j.toxrep.2019.03.005