Abstract
It is well known that immune response decreases with aging. Salidroside (SDS), an antioxidant component isolated from the traditional Chinese medicine roseroot Rhodiola rosea, has been demonstrated to possess potent anti-aging and health-promoting activities. However, the mechanism underlying these activities is poorly understood. In this study, we clearly demonstrated that (1) dietary intake of SDS induced a considerable increase in total T cells (CD3+) and T helper cells (CD4+) in aged (21 months old) Wistar male rats; (2) SDS supplementation significantly increased the DTH response, a T cell-mediated immune response, in aged rats; and (3) SDS supplementation remarkably promoted the production of total anti-KLH IgG, anti-KLH IgG1, and anti-KLH IgG2α in aged rats without disturbing immune homeostasis. These indicate that SDS is able to counteract immunosenescence, thereby resulting in rejuvenation. Practically, SDS may be used to help the elderly to generate an improved response to vaccine with stronger humoral and cell-mediated immune responses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bogden JD, Louria DB (1999) Aging and the immune system: the role of micronutrient nutrition. Nutrition 15(7–8):593–595. doi:10.1016/S0899-9007(99)00093-3
Bogden JD, Bendich A, Kemp FW, Bruening KS, Shurnick JH, Denny T, Baker H, Louria DB (1994) Daily micronutrient supplements enhance delayed-hypersensitivity skin test responses in older people. Am J Clin Nutr 60(3):437–447
Chakravarti B, Abraham GN (1999) Aging and T-cell-mediated immunity. Mech Ageing Dev 108(3):183–206. doi:10.1016/S0047-6374(99)00009-3
Cohn JR, Hohl CA, Buckley CE (1983) The relationship between cutaneous cellular immune responsiveness and mortality in a nursing-home population. J Am Geriatr Soc 31(12):808–809
Du B, Yan T, Ma Y, Wang Q, Yang W (2009) Effects of salidroside on hematological system in rats and mice. Chinese J Experiment Trad Med Form 15:51–54
Frasca D, Riley RL, Blomberg BB (2005) Humoral immune response and B-cell functions including immunoglobulin class switch are downregulated in aged mice and humans. Semin Immunol 17(5):378–384. doi:10.1016/j.smim.2005.05.005
Gomez CR, Nomellini V, Faunce DE, Kovacs EJ (2008) Innate immunity and aging. Exp Gerontol 43(8):718–728. doi:10.1016/j.exger.2008.05.016
Guan S, Wang W, Lu J, Qian WH, Huang GR, Deng XM, Wang XL (2011) Salidroside attenuates hydrogen peroxide-induced cell damage through a cAMP-dependent pathway. Molecules 16(4):3371–3379. doi:10.3390/molecules16043371
Hayek MG, Han SN, Wu D, Watkins BA, Meydani M, Dorsey JL, Smith DE, Meydani SN (1999) Dietary conjugated linoleic acid influences the immune response of young and old C57BL/6NCrlBR mice. J Nutr 129(1):32–38
Haynes L, Maue AC (2009) Effects of aging on T cell function. Curr Opin Immunol 21(4):414–417. doi:10.1016/j.coi.2009.05.009
Kanupriya D, Prasad D, Ram MS, Kumar R, Sawhney RC, Sharma SK, Ilavazhagan G, Kumar D, Banerjee PK (2005) Cytoprotective and antioxidant activity of Rhodiola imbricata against tert-butyl hydroperoxide induced oxidative injury in U-937 human macrophages. Mol Cell Biochem 275(1–2):1–6. doi:10.1007/s11010-005-7637-1
Kelly GS (2001) Rhodiola rosea: a possible plant adaptogen. Alternative Med Rev 6(3):293–302
Kemp FW, DeCandia J, Li WJ, Bruening K, Baker H, Rigassio D, Bendich A, Bogden JD (2002) Relationships between immunity and dietary and serum antioxidants, trace metals, B vitamins, and homocysteine in elderly men and women. Nutr Res 22(1–2):45–53. doi:10.1016/S0271-5317(01)00373-6
Kovacs EJ, Palmer JL, Fortin CF, Fulop T Jr, Goldstein DR, Linton PJ (2009) Aging and innate immunity in the mouse: impact of intrinsic and extrinsic factors. Trends Immunol 30(7):319–324. doi:10.1016/j.it.2009.03.012
Kumar R, Burns EA (2008) Age-related decline in immunity: implications for vaccine responsiveness. Expet Rev Vaccine 7(4):467–479. doi:10.1586/14760584.7.4.467
Linton PJ, Dorshkind K (2004) Age-related changes in lymphocyte development and function. Nat Immunol 5(2):133–139. doi:10.1038/ni1033
Ma L, Cai DL, Li HX, Tong BD, Wang Y, Pei SP (2009) Protective effects of salidroside on oxidative damage in fatigue mice. Zhong Xi Yi Jie He Xue Bao 7(3):237–241. doi:10.3736/jcim20090308
Mao GX, Deng HB, Yuan LG, Li DD, Li YY, Wang Z (2010) Protective role of salidroside against aging in a mouse model induced by d-galactose. Biomed Environ Sci 23(2):161–166. doi:10.1016/S0895-3988(10)60047-5
McGlauchlen KS, Vogel LA (2003) Ineffective humoral immunity in the elderly. Microb Infect 5(13):1279–1284. doi:10.1016/j.micinf.2003.09.001
Meakins JL, Pietsch JB, Bubenick O, Kelly R, Rode H, Gordon J, MacLean LD (1977) Delayed hypersensitivity: indicator of acquired failure of host defenses in sepsis and trauma. Ann Surg 186(3):241–250
Meydani SN, Meydani M, Blumberg JB, Leka LS, Siber G, Loszewski R, Thompson C, Pedrosa MC, Diamond RD, Stollar BD (1997) Vitamin E supplementation and in vivo immune response in healthy elderly subjects. A randomized controlled trial. JAMA 277(17):1380–1386
Pallast EG, Schouten EG, de Waart FG, Fonk HC, Doekes G, von Blomberg BM, Kok FJ (1999) Effect of 50- and 100-mg vitamin E supplements on cellular immune function in noninstitutionalized elderly persons. Am J Clin Nutr 69(6):1273–1281
Scherer K, Bircher AJ (2010) Danger signs in drug hypersensitivity. Med Clin North Am 94(4):681–689. doi:10.1016/j.mcna.2010.04.007
Schriner SE, Avanesian A, Liu YX, Luesch H, Jafari M (2009) Protection of human cultured cells against oxidative stress by Rhodiola rosea without activation of antioxidant defenses. Free Radic Biol Med 47(5):577–584. doi:10.1016/j.freeradbiomed.2009.05.025
Scrimshaw NS, SanGiovanni JP (1997) Synergism of nutrition, infection, and immunity: an overview. Am J Clin Nutr 66(2):S464–S477
Skopinska-Rozewska E, Malinowski M, Wasiutynski A, Sommer E, Furmanowa M, Mazurkiewicz M, Siwicki AK (2008) The influence of Rhodiola quadrifida 50% hydro-alcoholic extract and salidroside on tumor-induced angiogenesis in mice. Pol J Vet Sci 11(2):97–104
Smith TP, Kennedy SL, Fleshner M (2004) Influence of age and physical activity on the primary in vivo antibody and T cell-mediated responses in men. J Appl Physiol 97(2):491–498. doi:10.1152/japplphysiol.01404.2003
Snapper CM, Mond JJ (1993) Towards a comprehensive view of immunoglobulin class switching. Immunol Today 14:15–17. doi:10.1016/0167-5699(93)90318-F
Solana R, Pawelec G, Tarazona R (2006) Aging and innate immunity. Immunity 24(5):491–494. doi:10.1016/j.immuni.2006.05.003
Vidal K, Benyacoub J, Sanchez-Garcia J, Foata F, Segura-Roggero I, Serrant P, Moser M, Blum S (2010) Intake of a milk-based wolfberry formulation enhances the immune response of young-adult and aged mice. Rejuv Res 13(1):47–53. doi:10.1089/rej.2009.0895
Vos AP, Haarman M, Buco A, Govers M, Knol J, Garssen J, Stahl B, Boehm G, M’Rabet L (2006) A specific prebiotic oligosaccharide mixture stimulates delayed-type hypersensitivity in a murine influenza vaccination model. Inter Immunopharmacol 6(8):1277–1286. doi:10.1016/j.intimp. 2006.03.010
Wang H, Ding Y, Zhou J, Sun X, Wang S (2009) The in vitro and in vivo antiviral effects of salidroside from Rhodiola rosea L. against Coxsackievirus B3. Phytomedicine 16(2–3):146–155. doi:10.1016/j.phymed.2008.07.013
Wayne SJ, Rhyne RL, Garry PJ, Goodwin JS (1990) Cell-mediated immunity as a predictor of morbidity and mortality in subjects over 60. J Gerontol 45(2):M45–M48. doi:10.1093/geronj/45.2.M45
Weng NP (2006) Aging of the immune system: how much can the adaptive immune system adapt? Immunity 24(5):495–499. doi:10.1016/j.immuni.2006.05.001
Wu D, Han SN, Bronson RT, Smith DE, Meydani SN (1998) Dietary supplementation with mushroom-derived protein-bound glucan does not enhance immune function in young and old mice. J Nutr 128(2):193–197
Wu TJ, Zhou HP, Jin ZX, Bi SH, Yang XL, Yi DH, Liu WY (2009) Cardioprotection of salidroside from ischemia/reperfusion injury by increasing N-acetylglucosamine linkage to cellular proteins. Eur J Pharmacol 613(1–3):93–99. doi:10.1016/j.ejphar.2009.04.012
Ye YC, Chen QM, Jin KP, Zhou SX, Chai FL, Hai P (1993) Effect of salidroside on cultured myocardial cells anoxia/reoxygenation injuries. Zhongguo Yao Li Xue Bao 14(5):424–426
Yu S, Liu M, Gu XS, Ding F (2008) Neuroprotective effects of salidroside in the PC12 cell model exposed to hypoglycemia and serum limitation. Cell Mol Neurobiol 28(8):1067–1078. doi:10.1007/s10571-008-9284-z
Zhang L, Yu H, Sun Y, Lin X, Chen B, Tan C, Cao G, Wang Z (2007) Protective effects of salidroside on hydrogen peroxide-induced apoptosis in SH-SY5Y human neuroblastoma cells. Eur J Pharmacol 564(1–3):18–25. doi:10.1016/j.ejphar.2007.01.089
Zhu Y, Shi YP, Wu D, Ji YJ, Wang X, Chen HL, Wu SS, Huang DJ, Jiang W (2011) Salidroside protects against hydrogen peroxide-induced injury in cardiac H9c2 cells via PI3K-Akt dependent pathway. DNA Cell Biol 30(10):809–819. doi:10.1089/dna.2010.1183
Acknowledgments
The authors thank Ms. Jie Ma and Mr. Hongmiao Wang for their aids in collection of the blood and tissues of the animals. The authors also thank Dr. Gamal El-Sokkary for his valuable comments and suggestions on this paper. This work was supported in part by a grant (2012CB114404) of Ministry of Science and Technology (MOST) of China.
Author information
Authors and Affiliations
Corresponding author
Additional information
Linlin Lu and Jiangshui Yuan contributed equally to this work.
About this article
Cite this article
Lu, L., Yuan, J. & Zhang, S. Rejuvenating activity of salidroside (SDS): dietary intake of SDS enhances the immune response of aged rats. AGE 35, 637–646 (2013). https://doi.org/10.1007/s11357-012-9394-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11357-012-9394-x