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Journal of Immunology Research
Volume 2017, Article ID 3780572, 9 pages
https://doi.org/10.1155/2017/3780572
Review Article

Are the Therapeutic Effects of Huangqi (Astragalus membranaceus) on Diabetic Nephropathy Correlated with Its Regulation of Macrophage iNOS Activity?

1Department of Pharmacy, Shanxi Provincial People’s Hospital, Shanxi Medical University, Taiyuan 030012, China
2Department of Endocrinology, Shanxi Provincial People’s Hospital, Shanxi Medical University, Taiyuan 030012, China
3School of Pharmacy, China Pharmaceutical University, Nanjing 211198, China
4Department of Medical Record & Statistics, Shanxi Provincial People’s Hospital, Shanxi Medical University, Taiyuan 030012, China
5State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, China
6School of Health and Human Sciences, Southern Cross University, Military Rd, Lismore, NSW 2480, Australia
7Department of Nephrology, Shanxi Provincial People’s Hospital, Shanxi Medical University, Shanxi Kidney Disease Institute, No. 29 Shuangtasi Street, Taiyuan, Shanxi 030012, China

Correspondence should be addressed to Linda Banbury; moc.liamg@36yrubnabkl and Rongshan Li; moc.361@31ilnahsgnor

Received 6 July 2017; Revised 19 September 2017; Accepted 26 September 2017; Published 8 November 2017

Academic Editor: Hao Liu

Copyright © 2017 Hui Liao et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. E. Mogensen, C. K. Christensen, and E. Vittinghus, “The stages in diabetic renal disease: with emphasis on the stage of incipient diabetic nephropathy,” Diabetes, vol. 32, Supplement 2, pp. 64–78, 1983. View at Publisher · View at Google Scholar
  2. M. Garsen, A. L. Rops, T. J. Rabelink, J. H. Berden, and J. van der Vlag, “The role of heparanase and the endothelial glycocalyx in the development of proteinuria,” Nephrology Dialysis Transplantation, vol. 29, no. 1, pp. 49–55, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. Z. S. Wang, F. Xiong, X. H. Xie, D. Chen, J. H. Pan, and L. Cheng, “Astragaloside IV attenuates proteinuria in streptozotocin-induced diabetic nephropathy via the inhibition of endoplasmic reticulum stress,” BMC Nephrology, vol. 16, p. 44, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. L. Petrica, S. Ursoniu, F. Gadalean et al., “Urinary podocyte-associated mRNA levels correlate with proximal tubule dysfunction in early diabetic nephropathy of type 2 diabetes mellitus,” Diabetology & Metabolic Syndrome, vol. 9, no. 1, p. 31, 2017. View at Publisher · View at Google Scholar
  5. Z. Wang, M. Wei, M. Wang et al., “Inhibition of macrophage migration inhibitory factor reduces diabetic nephropathy in type II diabetes mice,” Inflammation, vol. 37, no. 6, pp. 2020–2029, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. O. M. Pena, J. Pistolic, D. Raj, C. D. Fjell, and R. E. Hancock, “Endotoxin tolerance represents a distinctive state of alternative polarization (M2) in human mononuclear cells,” The Journal of Immunology, vol. 186, no. 12, pp. 7243–7254, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. S. J. Tao, Z. N. Yin, Z. Q. Xu, W. H. Song, and H. Tan, “Influence of astragalus injection on serum type IV collagen and transforming growth factor-β1 in diabetic nephropathy patients,” Clinical Medicine of China, vol. 20, no. 3, pp. 217–219, 2004. View at Google Scholar
  8. F. Ren and H. Q. Xu, “Systematic review of the effectiveness and safety of Huangqi injection in treating diabetic nephropathy,” Western Journal of Traditional Chinese Medicine, vol. 27, no. 1, pp. 77–90, 2014. View at Google Scholar
  9. Y. Liu, L. Zhou, Y. Xiao, R. Luo, and X. S. Zhao, “The efficacy of ACEI or ARB combination with astragalus injection on early-stage diabetic nephropathy: a meta-analysis,” Journal of Tropical Medicine, vol. 13, no. 5, pp. 611–615, 2013. View at Google Scholar
  10. X. N. Shang, Systematic Review of Astragalus Injection Combined with ACEI or ARB in the Treatment of Stage III and IV Diabetic Nephropathy, Beijing University of Chinese Medicine, 2017.
  11. J. Jin, Y. L. Zhu, and L. J. Zeng, “Meta-analysis of Huangqi injection in the early stage of diabetic nephropathy,” Herald of Medicine, vol. 32, Supplement, pp. 257–261, 2013. View at Google Scholar
  12. M. Li, W. Wang, J. Xue, Y. Gu, and S. Lin, “Meta-analysis of the clinical value of Astragalus membranaceus in diabetic nephropathy,” Journal of Ethnopharmacology, vol. 133, no. 2, pp. 412–419, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Y. Ouyang, “Clinical study of Astragalus injection combined with atorvastatin calcium in the treatment of diabetic nephropathy,” China Prescription Drug, vol. 13, no. 8, pp. 5–7, 2015. View at Google Scholar
  14. W. J. Pan, G. L. Shen, and W. S. Liu, “Analysis of 120 cases of diabetic nephropathy treated by Astragalus injection combined with Chinese herbal decoction enema,” Acta Academiae Medicinae Weifang, vol. 25, no. 6, pp. 428–430, 2003. View at Google Scholar
  15. Y. Yang, F. S. Di, and K. J. Li, “Clinical observation of combined treatment of diabetic nephropathy with Huangqi Danshen injection and captopril,” Journal of Tianjin Medical University, vol. 6, no. 1, pp. 79–81, 2000. View at Google Scholar
  16. Z. J. Jia, J. Wang, and A. Zhang, “Clinical observation of Xueshuantong and Huangqi injection in the treatment of diabetic nephropathy,” Journal of Shandong University of Traditional Chinese Medicine, vol. 26, no. 5, pp. 361-362, 2002. View at Google Scholar
  17. S. Y. Yuan, Clinical Research of Acupuncture Point Injection of Chinese Medicine with Lotensin Treat Diabetic Nephropathy, Hubei University of Chinese Medicine, 2010.
  18. L. N. Wang, X. Z. Tang, and P. P. Chen, “Clinical effect of losartan combined with Astragalus injection on diabetic nephropathy,” Chinese Journal of Integrated Traditional and Western Nephrology, vol. 4, no. 8, pp. 471-472, 2003. View at Google Scholar
  19. F. Wu, Z. Y. Cai, K. L, B. Shen, J. Y. Ou, and X. L. Fei, “Effects of Astragalus injection on chronic inflammation and malnutrition in patients with chronic renal failure,” Chinese Journal of Traditional Medical Science and Technology, vol. 15, no. 4, p. 304, 2008. View at Google Scholar
  20. X. X. Cheng and J. Wang, “Effect of Astragalus injection on serum cytokines in patients with chronic renal failure,” Chinese Journal of Traditional Medical Science and Technology, vol. 8, no. 3, p. 178, 2001. View at Google Scholar
  21. J. H. Liu, H. X. Deng, X. Y. Yao, Y. H. He, B. Han, and Y. J. Peng, “Effect of Astragalus injection on immune function of chronic renal failure patients undergoing maintenance hemodialysis,” Study Journal of Traditional Chinese Medicine, vol. 19, no. 6, pp. 625-626, 2001. View at Google Scholar
  22. F. J. Shan, T. Z. Sun, K. Qi, G. L. Chen, W. S. Zhang, and X. Y. Li, “Observation on 482 cases of chronic renal failure were treated with Milkvetch,” Clinical Journal of Medical Officer, vol. 32, no. 4, pp. 22-23, 2004. View at Google Scholar
  23. L. Qiu and R. Q. Li, “Clinical observation of sodium ferulate and Astragalus injection in the treatment of chronic renal failure,” Modern Journal of Integrated Traditional Chinese and Western Medicine, vol. 17, no. 12, pp. 1850-1851, 2008. View at Google Scholar
  24. X. P. Zhu, J. X. Lin, X. H. Wang, and Y. H. Tang, “Effect of renal failure tincture and Astragalus injection on blood rheology and T lymphocyte subsets in hemodialysis patients with end-stage renal disease,” Shanghai Journal of Traditional Chinese Medicine, vol. 46, no. 7, pp. 20-21, 2000. View at Google Scholar
  25. Y. G. Wang, X. J. An, and X. Z. Wu, “Therapeutic effect of Astragalus injection on diabetic nephropathy complicated with chronic renal failure,” Chinese Journal of Integrated Traditional and Western Medicine in Intensive and Critical Care, vol. 6, no. 5, p. 230, 1999. View at Google Scholar
  26. Y. Li, “Curative effect analysis of Astragalus injection combined with acupoint injection in treating chronic renal failure,” Clinical Journal of Chinese Medicine, vol. 8, no. 18, pp. 119-120, 2016. View at Google Scholar
  27. R. X. Jing, “Clinical observation on 106 cases of chronic renal failure treated with Astragalus injection,” Journal of China Traditional Chinese Medicine Information, vol. 3, no. 16, pp. 67-68, 2011. View at Google Scholar
  28. H. S. Yang, “Clinical analysis of losartan combined with Astragalus injection in the treatment of chronic renal failure,” Asia-Pacific Traditional Medicine, vol. 5, no. 9, pp. 133-134, 2009. View at Google Scholar
  29. J. T. Lu, Y. Yang, and M. Z. Chen, “Effect of astragalus polysaccharides on IL-1, NO and TNF-α secreted by lipopolysaccharide-induced normal rat peritoneal macrophages,” Acta Universitatis Medicinalis Anhui, vol. 39, no. 2, pp. 139–141, 2004. View at Google Scholar
  30. L. Xu, X. J. He, W. Chai, D. H. Ju, A. P. Lv, and C. Y. Yu, “Effect of Astragalus polysaccharides on TNF-α, IL-1β and NO by lipopolysaccharide-activated macrophages,” Chinese Journal of Basic Medicine in Traditional Chinese Medicine, vol. 17, no. 5, pp. 503-504, 2011. View at Google Scholar
  31. H. Liao, X. M. Wang, X. K. Lv, H. P. Liang, and L. Hu, “Impacts of Astragalus on nitric oxide generated from macrophages in the mice activated with lipopolysaccharide,” World Journal of Integrated Traditional and Western Medicine, vol. 9, no. 1, pp. 33–36, 2014. View at Google Scholar
  32. X. Zhang, Z. Guo, C. Zhang et al., “Effect of total flavonoids of Astragalus on secretion levels of cytokines in LPS-induced RAW264.7 cells,” Chinese Veterinary Science, vol. 45, no. 3, pp. 321–324, 2015. View at Google Scholar
  33. Y. Wang, T. Ren, L. Zheng, H. Chen, J. K. Ko, and K. K. Auyeung, “Astragalus saponins inhibits lipopolysaccharide-induced inflammation in mouse macrophages,” The American Journal of Chinese Medicine, vol. 44, no. 3, pp. 579–593, 2016. View at Publisher · View at Google Scholar · View at Scopus
  34. W. Chen, Y. Y. Zhang, Z. Wang, X. H. Luo, W. C. Sun, and H. B. Wang, “Phenolic derivatives from Radix Astragali and their anti-inflammatory activities,” Natural Product Communications, vol. 11, no. 9, pp. 1577–1580, 2014. View at Google Scholar
  35. W. Li, Y. N. Sun, X. T. Yan et al., “NF-κB inhibitory activity of sucrose fatty acid esters and related constituents from Astragalus membranaceus,” Journal of Agricultural and Food Chemistry, vol. 61, no. 29, pp. 7081–7088, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Ryu, E. H. Kim, M. Chun et al., “Astragali radix elicits anti-inflammation via activation of MKP-1, concomitant with attenuation of p38 and Erk,” Journal of Ethnopharmacology, vol. 115, no. 2, pp. 184–193, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Y. Lee, H. J. Noh, J. Choi et al., “Anti-inflammatory cycloartane-type saponins of Astragalus membranaceus,” Molecules, vol. 18, no. 4, pp. 3725–3732, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. P. K. Lai, J. Y. Chan, L. Cheng et al., “Isolation of anti-inflammatory fractions and compounds from the root of Astragalus membranaceus,” Phytotherapy Research, vol. 27, no. 4, pp. 581–587, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. L. J. Zhang, H. K. Liu, P. C. Hsiao et al., “New isoflavonoid glycosides and related constituents from astragali radix (Astragalus membranaceus) and their inhibitory activity on nitric oxide production,” Journal of Agricultural and Food Chemistry, vol. 59, no. 4, pp. 1131–1137, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. W. W. Chao, Y. H. Kuo, W. C. Li, and B. F. Lin, “The production of nitric oxide and prostaglandin E2 in peritoneal macrophages is inhibited by Andrographis paniculata, Angelica sinensis and Morus alba ethyl acetate fractions,” Journal of Ethnopharmacology, vol. 122, no. 1, pp. 68–75, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. J. H. Wang, J. C. Dong, J. X. Zhao, S. Z. Jin, H. Y. Zhang, and S. Y. Zhang, “Effects of different molecule weight astragalus polysacharin isolated from annual Astragalus membraneaceus on expressions of inflammatory cytokines in RAW264.7 cells,” Journal of Jilin University, vol. 37, no. 6, pp. 1051–1056, 2011. View at Google Scholar
  42. L. Chen, M. Zhang, X. L. Xie, and Y. M. Sheng, “Influence of component compatibility of Astragalus membranaceus on the immunocompetence of peritoneal macrophages in mice,” Chinese Journal of Hospital Pharmacy, vol. 34, no. 10, pp. 787–790, 2014. View at Google Scholar
  43. J. F. Yao, Z. X. Wang, X. Y. Zhang, and R. F. Zhang, “Study on immunomodulatory effect of Astragalus polysaccharide on mice peritoneal macrophage,” Journal of Henan University, vol. 24, no. 1, pp. 34–36, 2005. View at Google Scholar
  44. X. M. Yang, T. Y. Zhang, C. L. Zhu, and L. Lin, “Activating effect of astragalus saponin on mouse peritoneal macrophages in vitro,” Chinese Journal of Pathophysiology, vol. 24, no. 8, pp. 1625–1628, 2008. View at Google Scholar
  45. J. Zhu, Z. Xiao, Y. S. Shen, and G. Y. Wu, “The role of nuclear factor-kappa B in the induction of nitric oxide and tumor necrosis factor-alpha by Astragalus Mongholicus polysaccharides in macrophages,” Chinese Journal of Microbiology and Immunology, vol. 30, no. 6, pp. 511–515, 2010. View at Google Scholar
  46. X. Lv, D. Chen, L. Yang et al., “Comparative studies on the immunoregulatory effects of three polysaccharides using high content imaging system,” International Journal of Biological Macromolecules, vol. 86, pp. 28–42, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. W. Wei, H. T. Xiao, W. R. Bao et al., “TLR-4 may mediate signaling pathways of Astragalus polysaccharide RAP induced cytokine expression of RAW264.7 cells,” Journal of Ethnopharmacology, vol. 179, pp. 243–252, 2016. View at Publisher · View at Google Scholar · View at Scopus
  48. L. H. Zhao, Z. X. Ma, J. Zhu, X. H. Yu, and D. P. Weng, “Characterization of polysaccharide from Astragalus radix as the macrophage stimulator,” Cellular Immunology, vol. 271, no. 2, pp. 329–334, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Y. Lee and Y. J. Jeon, “Macrophage activation by polysaccharide isolated from Astragalus membranaceus,” International Immunopharmacology, vol. 5, no. 7-8, pp. 1225–1233, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Zhang, Z. Sun, and C. M. Jiang, “Effect of Astragalus injection on peritoneal macrophages in peritoneal dialysis patients,” Journal of Nanjing TCM University, vol. 23, no. 5, pp. 319–321, 2007. View at Google Scholar
  51. F. Xiang, Y. Y. Zhang, H. Yuan, Y. Zhang, and Y. Q. Shao, “2000–2014 diabetes control policy changes in China,” Chinese Journal of Prevention and Control of Chronic Diseases, vol. 24, no. 4, pp. 309–311, 2016. View at Google Scholar
  52. L. Zhang, J. Long, W. Jiang et al., “Trends in chronic kidney disease in China,” New England Journal of Medicine, vol. 375, no. 9, pp. 905-906, 2016. View at Publisher · View at Google Scholar · View at Scopus
  53. Q. Li, H. M. Zhang, Y. T. Fei, J. M. Xing, H. Luo, and J. P. Liu, “Treatment of diabetic nephropathy by integrative medicine: a multi-center prospective cohort study,” Chinese Journal of Integrated Traditional and Western Medicine, vol. 32, no. 3, pp. 317–321, 2012. View at Google Scholar
  54. J. H. Tang, Y. L. Jiang, and M. Q. Huang, “Clinical observation of Astragalus injection on hepatitis B surface antigen carriers,” Jiangsu Medical Journal, vol. 5, no. 4, pp. 26–28, 1979. View at Google Scholar
  55. C. Zhang, C. Zhu, Y. Ling et al., “The clinical value of Huangqi injection in the treatment of leucopenia: a meta-analysis of clinical controlled trials,” PLoS One, vol. 8, no. 12, article e83123, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. Y. L. Piao and X. C. Liang, “Astragalus membranaceus injection combined with conventional treatment for viral myocarditis: a systematic review of randomized controlled trials,” Chinese Journal of Integrative Medicine, vol. 20, no. 10, pp. 787–791, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. Committee of national pharmacopoeia standard room, “Quality standard of Huangqi injection,” Drug Standards of China, vol. 3, no. 1, pp. 32–34, 2002. View at Google Scholar
  58. L. H. Jian, J. Xia, Y. Y. Shen, J. Lin, K. Wang, and S. Ji, “Study of relative molecular mass of polysaccharides in Huangqi injection by high performance gel permeation chromatography,” Chinese Journal of Pharmaceutical Analysis, vol. 30, no. 11, pp. 2037–2039, 2010. View at Google Scholar
  59. L. H. Jian, H. L. Wen, J. Xia, K. Wang, and S. Ji, “Improvement of qualitative and quantitative of analyses methods of Astragalus injection,” Chinese Traditional Patent Medicine, vol. 33, no. 11, pp. 2018–2020, 2011. View at Google Scholar
  60. J. H. Chu, C. Y. Li, G. L. Dai, and W. Z. Ju, “Simultaneous determination of five components in Astragalus injection and Astragalus oral liquid by LC-MS-MS,” Chinese Traditional Patent Medicine, vol. 37, no. 12, pp. 2647–2651, 2015. View at Google Scholar
  61. F. Zhang, Y. Wei, Y. Zhou et al., “Pharmacokinetics and hepatic uptake of gliquidone affected by Huangqi injection,” European Journal of Drug Metabolism and Pharmacokinetics, vol. 39, no. 4, pp. 255–261, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. T. S. Gao, S. J. Yu, Y. L. Xu, and L. J. Ma, “Treatment of 30 cases of early diabetic nephropathy with Astragalus injection,” Medical Journal of Liaoning, vol. 12, no. 1, pp. 49-50, 1998. View at Google Scholar
  63. S. Lee, S. Huen, H. Nishio et al., “Distinct macrophage phenotypes contribute to kidney injury and repair,” Journal of the American Society of Nephrology, vol. 22, no. 2, pp. 317–326, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. Z. H. Qi, S. Y. Lin, and Y. F. Huang, “A study on Astragalus Membranaceus (Fisch.) bge, in regulating renal hemodynamics in early diabetic rat,” Chinese Journal of Diabetes, vol. 7, no. 3, pp. 147–149, 1999. View at Google Scholar
  65. N. Levin-laina, A. Iaina, and I. Raz, “The emerging role of NO and IGF-1 in early renal hypertrophy in STZ-induced diabetic rats,” Diabetes/Metabolism Research and Reviews, vol. 27, no. 3, pp. 235–243, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Trachtman, S. Futterweit, E. Pine, J. Mann, and E. Valderrama, “Chronic diabetic nephropathy: role of inducible nitric oxide synthase,” Pediatric Nephrology, vol. 17, no. 1, pp. 20–29, 2002. View at Publisher · View at Google Scholar · View at Scopus
  67. M. F. Sönmez and M. Dündar, “Ameliorative effects of pentoxifylline on NOS induced by diabetes in rat kidney,” Renal Failure, vol. 38, no. 4, pp. 605–613, 2016. View at Publisher · View at Google Scholar · View at Scopus
  68. M. G. Ferrini, S. Rivera, J. Moon, D. Vernet, J. Rajfer, and N. F. Gonzalez-Cadavid, “The genetic inactivation of inducible nitric oxide synthase (iNOS) intensifies fibrosis and oxidative stress in the penile corpora cavernosa in type 1 diabetes,” The Journal of Sexual Medicine, vol. 7, no. 9, pp. 3033–3044, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. F. Ren and H. Q. Xu, “Quality evaluation of the report for randomized controlled trials of Huangqi injection in treating diabetic nephropathy,” Western Journal of Traditional Chinese Medicine, vol. 26, no. 12, pp. 1–4, 2013. View at Google Scholar
  70. L. Zhou, Z. Liu, Z. Wang et al., “Astragalus polysaccharides exerts immunomodulatory effects via TLR4-mediated MyD88-dependent signaling pathway in vitro and in vivo,” Scientific Reports, vol. 7, article 44822, 2017. View at Publisher · View at Google Scholar
  71. M. Li, H. Li, F. Fang, X. Deng, and S. Ma, “Astragaloside IV attenuates cognitive impairments induced by transient cerebral ischemia and reperfusion in mice via anti-inflammatory mechanisms,” Neuroscience Letters, vol. 639, pp. 114–119, 2017. View at Publisher · View at Google Scholar
  72. L. L. Lv, P. M. Tang, C. J. Li et al., “The pattern recognition receptor, Mincle, is essential for maintaining the M1 macrophage phenotype in acute renal inflammation,” Kidney International, vol. 91, no. 3, pp. 587–602, 2017. View at Publisher · View at Google Scholar
  73. T. A. Wynn and K. M. Vannella, “Macrophages in tissue repair, regeneration, and fibrosis,” Immunity, vol. 44, no. 3, pp. 450–462, 2016. View at Publisher · View at Google Scholar · View at Scopus