Therapeutic effects of Salvia miltiorrhiza injection combined with telmisartan in patients with diabetic nephropathy by influencing collagen IV and fibronectin: A case-control study

Nie,Jie-Ming; Li,Hai-Feng

doi:10.3892/etm.2018.6654

Therapeutic effects of Salvia miltiorrhiza injection combined with telmisartan in patients with diabetic nephropathy by influencing collagen IV and fibronectin: A case-control study

Authors:
- Jie-Ming Nie
- Hai-Feng Li
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Affiliations: Department of Internal Medicine, Τhe Third Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong 510150, P.R. China, Department of Pharmaceutical Analysis, ALK-Abello A/S Guangzhou Office, Guangzhou, Guangdong 510620, P.R. China
Published online on: August 24, 2018 https://doi.org/10.3892/etm.2018.6654
Pages: 3405-3412
Copyright: © Nie et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Involvement of collagen IV (ColIV) and fibronectin (FN) in the occurrence and development of diabetic nephropathy (DN) and the effects of telmisartan and Salvia miltiorrhiza injection in the treatment of the patients were investigated. Two hundred and fifty-eight patients with stage IV DN were selected as the case group, and another 110 normal healthy subjects were incorporated as the control group. Involved patients were subdivided into different groups according to different treatment therapies; patients in the telmisartan group (T group) were given oral telmisartan; patients in the Salvia miltiorrhiza injection + telmisartan (S + T group) were administered with Salvia miltiorrhiza injection combined with telmisartan treatment, and there was a group of patients who received no intervention as the placebo group. After intervention, levels of glycemic indexes and renal damage indexes indicated downwards trends both in the T group and the S + T group when compared to the placebo group; besides, levels in the S + T group were much lower than those in the T group (all P<0.05). Additionally, in comparison among the above three intervention groups, differences in the fasting blood glucose, 2 h post-prandial blood glucose, glycosylated hemoglobin, blood urea nitrogen, serum creatinine and urinary albumin excretion rate were significant after treatment (all P<0.05). Further, before intervention, both Co1IV and FN in the urine were increased in the case group compared to the control group (all P<0.05). After intervention, both levels were apparently decreased. There were remarkable differences of Co1IV and FN levels in the urine when compared among three different intervention groups after treatment (P<0.05). Increased ColIV and FN levels may be partially responsible for the development of DN. Salvia miltiorrhiza injection with telmisartan have beneficial synergistic effects for DN patients through attenuating the increase in ColIV and FN, reversing hyperglycemia state and postponing ultrastructure changes of glomerular basement membrane.

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1	Crossland L, Askew D, Ware R, Cranstoun P, Mitchell P, Bryett A and Jackson C: Diabetic retinopathy screening and monitoring of early stage disease in Australian general practice: Tackling preventable blindness within a chronic care model. J Diabetes Res. 2016:84053952016. View Article : Google Scholar : PubMed/NCBI
2	Cobas RA, Santos B, da Silva PC, Neves R and Gomes MB: Progression to microalbuminuria in patients with type 1 diabetes: A seven-year prospective study. Diabetol Metab Syndr. 3:212011. View Article : Google Scholar : PubMed/NCBI
3	Reutens AT and Atkins RC: Epidemiology of diabetic nephropathy. Contrib Nephrol. 170:1–7. 2011. View Article : Google Scholar : PubMed/NCBI
4	Van Buren PN and Toto R: Hypertension in diabetic nephropathy: Epidemiology, mechanisms, and management. Adv Chronic Kidney Dis. 18:28–41. 2011. View Article : Google Scholar : PubMed/NCBI
5	Navarro-González JF and Mora-Fernández C: The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol. 19:433–442. 2008. View Article : Google Scholar : PubMed/NCBI
6	Zhou Z, Pausch F, Schlötzer-Schrehardt U, Brachvogel B and Pöschl E: Induction of initial steps of angiogenic differentiation and maturation of endothelial cells by pericytes in vitro and the role of collagen IV. Histochem Cell Biol. 145:511–525. 2016. View Article : Google Scholar : PubMed/NCBI
7	Behrens DT, Villone D, Koch M, Brunner G, Sorokin L, Robenek H, Bruckner-Tuderman L, Bruckner P and Hansen U: The epidermal basement membrane is a composite of separate laminin- or collagen IV-containing networks connected by aggregated perlecan, but not by nidogens. J Biol Chem. 287:18700–18709. 2012. View Article : Google Scholar : PubMed/NCBI
8	Rosado C, Bueno E, Fraile P, García-Cosmes P and González-Sarmiento R: A new mutation in the COL4A3 gene responsible for autosomal dominant Alport syndrome, which only generates hearing loss in some carriers. Eur J Med Genet. 58:35–38. 2015. View Article : Google Scholar : PubMed/NCBI
9	Yoneda Y, Haginoya K, Arai H, Yamaoka S, Tsurusaki Y, Doi H, Miyake N, Yokochi K, Osaka H, Kato M, et al: De novo and inherited mutations in COL4A2, encoding the type IV collagen α2 chain cause porencephaly. Am J Hum Genet. 90:86–90. 2012. View Article : Google Scholar : PubMed/NCBI
10	El-Mezayen HA, Habib S, Marzok HF and Saad MH: Diagnostic performance of collagen IV and laminin for the prediction of fibrosis and cirrhosis in chronic hepatitis C patients: A multicenter study. Eur J Gastroenterol Hepatol. 27:378–385. 2015. View Article : Google Scholar : PubMed/NCBI
11	Abrahamson DR, St John PL, Stroganova L, Zelenchuk A and Steenhard BM: Laminin and type IV collagen isoform substitutions occur in temporally and spatially distinct patterns in developing kidney glomerular basement membranes. J Histochem Cytochem. 61:706–718. 2013. View Article : Google Scholar : PubMed/NCBI
12	Ruggiero S, Cosgarea R, Potempa J, Potempa B, Eick S and Chiquet M: Cleavage of extracellular matrix in periodontitis: Gingipains differentially affect cell adhesion activities of fibronectin and tenascin-C. Biochim Biophys Acta. 1832:517–526. 2013. View Article : Google Scholar : PubMed/NCBI
13	Halper J and Kjaer M: Basic components of connective tissues and extracellular matrix: Elastin, fibrillin, fibulins, fibrinogen, fibronectin, laminin, tenascins and thrombospondins. Adv Exp Med Biol. 802:31–47. 2014. View Article : Google Scholar : PubMed/NCBI
14	Kang Y, Georgiou AI, MacFarlane RJ, Klontzas ME, Heliotis M, Tsiridis E and Mantalaris A: Fibronectin stimulates the osteogenic differentiation of murine embryonic stem cells. J Tissue Eng Regen Med. 11:1929–1940. 2017. View Article : Google Scholar : PubMed/NCBI
15	Sawicka KM, Seeliger M, Musaev T, Macri LK and Clark RA: Fibronectin interaction and enhancement of growth factors: Importance for wound healing. Adv Wound Care (New Rochelle). 4:469–478. 2015. View Article : Google Scholar : PubMed/NCBI
16	Linsley C, Wu B and Tawil B: The effect of fibrinogen, collagen type I, and fibronectin on mesenchymal stem cell growth and differentiation into osteoblasts. Tissue Eng Part A. 19:1416–1423. 2013. View Article : Google Scholar : PubMed/NCBI
17	Kenny HA, Chiang CY, White EA, Schryver EM, Habis M, Romero IL, Ladanyi A, Penicka CV, George J, Matlin K, et al: Mesothelial cells promote early ovarian cancer metastasis through fibronectin secretion. J Clin Invest. 124:4614–4628. 2014. View Article : Google Scholar : PubMed/NCBI
18	Mòdol T, Brice N, Ruiz de Galarreta M, García Garzón A, Iraburu MJ, Martínez-Irujo JJ and López-Zabalza MJ: Fibronectin peptides as potential regulators of hepatic fibrosis through apoptosis of hepatic stellate cells. J Cell Physiol. 230:546–553. 2015. View Article : Google Scholar : PubMed/NCBI
19	Toledo E, Hu FB, Estruch R, Buil-Cosiales P, Corella D, Salas-Salvadó J, Covas MI, Arós F, Gómez-Gracia E, Fiol M, et al: Effect of the Mediterranean diet on blood pressure in the PREDIMED trial: Results from a randomized controlled trial. BMC Med. 11:2072013. View Article : Google Scholar : PubMed/NCBI
20	Xiong X, Yang X, Liu W, Chu F, Wang P and Wang J: Trends in the treatment of hypertension from the perspective of traditional Chinese medicine. Evid Based Complement Alternat Med. 2013:2752792013. View Article : Google Scholar : PubMed/NCBI
21	Ebner T, Schänzle G, Weber W, Sent U and Elliott J: In vitro glucuronidation of the angiotensin II receptor antagonist telmisartan in the cat: A comparison with other species. J Vet Pharmacol Ther. 36:154–160. 2013. View Article : Google Scholar : PubMed/NCBI
22	Podymow T and Joseph G: Preconception and pregnancy management of women with diabetic nephropathy on angiotensin converting enzyme inhibitors. Clin Nephrol. 83:73–79. 2015. View Article : Google Scholar : PubMed/NCBI
23	Lewis G and Maxwell AP: Should women with diabetic nephropathy considering pregnancy continue ACE inhibitor or angiotensin II receptor blocker therapy until pregnancy is confirmed? Diabetologia. 57:1082–1083. 2014. View Article : Google Scholar : PubMed/NCBI
24	van Poppel PC, Breedveld P, Abbink EJ, Roelofs H, van Heerde W, Smits P, Lin W, Tan AH and Russel FG: Donders Ret alSalvia miltiorrhiza root water-extract (Danshen) has no beneficial effect on cardiovascular risk factors. A randomized double-blind cross-over trial. PLoS One. 10:e01286952015. View Article : Google Scholar : PubMed/NCBI
25	Zhou X, Chan K and Yeung JH: Herb-drug interactions with Danshen (Salvia miltiorrhiza): A review on the role of cytochrome P450 enzymes. Drug Metabol Drug Interact. 27:9–18. 2012. View Article : Google Scholar : PubMed/NCBI
26	Liu Y, Huang Y, Zhao C, Qin X, Zhu Q, Chen S and Qu J: Salvia miltiorrhiza injection on pulmonary heart disease: A systematic review and meta-analysis. Am J Chin Med. 42:1315–1331. 2014. View Article : Google Scholar : PubMed/NCBI
27	Luo J, Song W, Yang G, Xu H and Chen K: Compound Danshen (Salvia miltiorrhiza) dripping pill for coronary heart disease: An overview of systematic reviews. Am J Chin Med. 43:25–43. 2015. View Article : Google Scholar : PubMed/NCBI
28	Ge G, Zhang Q, Ma J, Qiao Z, Huang J, Cheng W and Wang H: Protective effect of Salvia miltiorrhiza aqueous extract on myocardium oxidative injury in ischemic-reperfusion rats. Gene. 546:97–103. 2014. View Article : Google Scholar : PubMed/NCBI
29	Mogensen C: Early diabetic renal involvement and nephropathy. Diabetes Annual. 3:306–324. 1987.
30	Upadhyaya HB, Vora MB, Nagar JG and Patel PB: Knowledge, attitude and practices toward pharmacovigilance and adverse drug reactions in postgraduate students of Tertiary Care Hospital in Gujarat. J Adv Pharm Technol Res. 6:29–34. 2015. View Article : Google Scholar : PubMed/NCBI
31	Goyal J, Khan ZY, Upadhyaya P, Goyal B and Jain S: Comparative study of high dose mono-therapy of amlodipine or telmisartan, and their low dose combination in mild to moderate hypertension. J Clin Diagn Res. 8:HC08–HC11. 2014.PubMed/NCBI
32	Huang JZ, Zheng FS and Yang Y: Clinical observation of telmisartan combined with tongxinluo capsules in the treatment of early diabetic nephropathy. China Pharm. 22:1101–1103. 2011.
33	Sato-Ηoriguchi C, Ogawa D, Wada J, Tachibana H, Kodera R, Eguchi J, Nakatsuka A, Terami N, Shikata K and Makino H: Telmisartan attenuates diabetic nephropathy by suppressing oxidative stress in db/db mice. Nephron Exp Nephrol. 121:e97–e108. 2012. View Article : Google Scholar : PubMed/NCBI
34	Bjornstad P, Snell-Bergeon JK, Rewers M, Jalal D, Chonchol MB, Johnson RJ and Maahs DM: Early diabetic nephropathy: A complication of reduced insulin sensitivity in type 1 diabetes. Diabetes Care. 36:3678–3683. 2013. View Article : Google Scholar : PubMed/NCBI
35	Kim BH, Lee ES, Choi R, Nawaboot J, Lee MY, Lee EY, Kim HS and Chung CH: Protective effects of curcumin on renal oxidative stress and lipid metabolism in a rat model of type 2 diabetic nephropathy. Yonsei Med J. 57:664–673. 2016. View Article : Google Scholar : PubMed/NCBI
36	Jha JC, Gray SP, Barit D, Okabe J, El-Osta A, Namikoshi T, Thallas-Bonke V, Wingler K, Szyndralewiez C, Heitz F, et al: Genetic targeting or pharmacologic inhibition of NADPH oxidase nox4 provides renoprotection in long-term diabetic nephropathy. J Am Soc Nephrol. 25:1237–1254. 2014. View Article : Google Scholar : PubMed/NCBI
37	Sun YM, Su Y, Li J and Wang LF: Recent advances in understanding the biochemical and molecular mechanism of diabetic nephropathy. Biochem Biophys Res Commun. 433:359–361. 2013. View Article : Google Scholar : PubMed/NCBI
38	Pichaiwong W, Hudkins KL, Wietecha T, Nguyen TQ, Tachaudomdach C, Li W, Askari B, Kobayashi T, O'Brien KD, Pippin JW, et al: Reversibility of structural and functional damage in a model of advanced diabetic nephropathy. J Am Soc Nephrol. 24:1088–1102. 2013. View Article : Google Scholar : PubMed/NCBI
39	Kolset SO, Reinholt FP and Jenssen T: Diabetic nephropathy and extracellular matrix. J Histochem Cytochem. 60:976–986. 2012. View Article : Google Scholar : PubMed/NCBI
40	Lenihan CR, Busque S, Derby G, Blouch K, Myers BD and Tan JC: Longitudinal study of living kidney donor glomerular dynamics after nephrectomy. J Clin Invest. 125:1311–1318. 2015. View Article : Google Scholar : PubMed/NCBI
41	Song KH, Park J, Park JH, Natarajan R and Ha H: Fractalkine and its receptor mediate extracellular matrix accumulation in diabetic nephropathy in mice. Diabetologia. 56:1661–1669. 2013. View Article : Google Scholar : PubMed/NCBI
42	Pieri M, Stefanou C, Zaravinos A, Erguler K, Stylianou K, Lapathitis G, Karaiskos C, Savva I, Paraskeva R, Dweep H, et al: Evidence for activation of the unfolded protein response in collagen IV nephropathies. J Am Soc Nephrol. 25:260–275. 2014. View Article : Google Scholar : PubMed/NCBI
43	Yap WT, Salvay DM, Silliman MA, Zhang X, Bannon ZG, Kaufman DB, Lowe WL Jr and Shea LD: Collagen IV-modified scaffolds improve islet survival and function and reduce time to euglycemia. Tissue Eng Part A. 19:2361–2372. 2013. View Article : Google Scholar : PubMed/NCBI
44	Yung S, Ng CY, Ho SK, Cheung KF, Chan KW, Zhang Q, Chau MK and Chan TM: Anti-dsDNA antibody induces soluble fibronectin secretion by proximal renal tubular epithelial cells and downstream increase of TGF-β1 and collagen synthesis. J Autoimmun. 58:111–122. 2015. View Article : Google Scholar : PubMed/NCBI
45	Tang O, Chen XM, Shen S, Hahn M and Pollock CA: miRNA-200b represses transforming growth factor-β1-induced EMT and fibronectin expression in kidney proximal tubular cells. Am J Physiol Renal Physiol. 304:F1266–F1273. 2013. View Article : Google Scholar : PubMed/NCBI
46	Knowles LM, Gurski LA, Maranchie JK and Pilch J: Fibronectin matrix formation is a prerequisite for colonization of kidney tumor cells in fibrin. J Cancer. 6:98–104. 2015. View Article : Google Scholar : PubMed/NCBI
47	Liu JQ, Lee TF, Miedzyblocki M, Chan GC, Bigam DL and Cheung PY: Effects of tanshinone IIA, a major component of Salvia miltiorrhiza, on platelet aggregation in healthy newborn piglets. J Ethnopharmacol. 137:44–49. 2011. View Article : Google Scholar : PubMed/NCBI
48	Ahn YM, Kim SK, Lee SH, Ahn SY, Kang SW, Chung JH, Kim SD and Lee BC: Renoprotective effect of Tanshinone IIA, an active component of Salvia miltiorrhiza, on rats with chronic kidney disease. Phytother Res. 24:1886–1892. 2010. View Article : Google Scholar : PubMed/NCBI
49	Wang JG, Pimenta E and Chwallek F: Comparative review of the blood pressure-lowering and cardiovascular benefits of telmisartan and perindopril. Vasc Health Risk Manag. 10:189–200. 2014. View Article : Google Scholar : PubMed/NCBI