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The Structure and Nephroprotective Activity of Oligo-Porphyran on Glycerol-Induced Acute Renal Failure in Rats

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The Structure and Nephroprotective Activity of Oligo-Porphyran on Glycerol-Induced Acute Renal Failure in Rats marine drugs Article The Structure and Nephroprotective Activity of Oligo-Porphyran on Glycerol-Induced Acute Renal Failure in Rats Jing Wang 1,2, Yun Hou 1,3, Delin Duan 1,2,4 and Quanbin Zhang 1,2,* 1 Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, Shandong, China; [email protected] (J.W.); [email protected] (Y.H.); [email protected] (D.D.) 2 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China 3 Graduate University of the Chinese Academy of Sciences, Beijing 100049, China 4 State Key Lab of Seaweed Bioactive Substances, Qingdao 266500, China * Correspondence: [email protected]; Tel.: +86-532-8289-8708 Academic Editor: Keith B. Glaser Received: 1 February 2017; Accepted: 4 May 2017; Published: 9 May 2017 Abstract: Porphyran is a sulfate galactan in the cell wall of Porphyra. Its acid hydrolysis product, oligo-porphyran (OP), was prepared and the structure studied by electrospray ionization time-of-flight mass spectrometry (ESI-TOF-MS). This oligosaccharide was mainly composed of monosulfate-oligo-galactan, disufate-oligo-galactan, trisulfate-oligo-galactan, trisulfate oligo-methyl-galactan, and 3,6-anhydrogalactose with the degree of polymerization ranging from 1 to 8. The effects of OP were investigated in the glycerol-induced acute renal failure (ARF) model. Compared with the normal group, rats from the glycerol-induced group exhibited collecting duct and medullary ascending limb dilation and casts. The OP-treated group exerted a protective effect against glycerol-induced changes. The results showed that the administration of OP markedly decreased mortality in female ARF rats. For male ARF rats, all of which survived, OP significantly decreased the blood urea nitrogen and serum creatinine levels. Ion levels in plasma and urine were significantly changed in ARF rats, whereas OP treatment almost recovered ion levels back to normal. This study showed a noticeable renal morphologic and functional protection by OP in glycerol-induced ARF rats. Keywords: sulfated galactan; oligo-porphyran; acute renal failure; gender difference 1. Introduction Acute renal failure (ARF) is a syndrome characterized by a rapid loss of kidney function [1]. During ARF, tubular fluid flow rate and glomerular filtration rate decrease rapidly. Subsequently, the kidney is unable to produce sufficient amounts of urine, and nitrogen-containing waste substances accumulate in the blood [2–4]. ARF is a contributor to many other diseases, including cardiovascular diseases, hypertension, and diabetes mellitus [5]. This syndrome has a major impact on the life quality of patients, and it is even life-threatening in some conditions [6]. Porphyran, with a linear backbone of alternating 3-linked β-D-galactose and 4-linked α-L-galactose-6-sulfate or 3,6-anhydro-α-L-galactose (3,6-AG) units [7], is the main polysaccharide in the cell wall of Porphyra. Porphyran has various biological activities, which are mainly attributed to its sulfated group [8,9]. In our previous study, we found that the sulfated polysaccharides from Laminaria and its hydrolysis products had protective effect on the rats with renal impairment [10,11]. One of an important factor for glycerol-induced renal injury is oxidative stress [12–14]. Porphyran has been proven to have strong antioxidant activity in vitro, however, few people studied its inhibition Mar. Drugs 2017, 15, 135; doi:10.3390/md15050135 www.mdpi.com/journal/marinedrugs Mar. Drugs 2017, 15, 135 2 of 13 has been proven to have strong antioxidant activity in vitro, however, few people studied its Mar. Drugs 2017, 15, 135 2 of 13 inhibition effect on ARF. Glycerol was a common agent for the induction of ARF in vivo and can lead to renal oxidative stress, as previously reported [15]. Therefore, the protective effect on glycerol‐ inducedeffect on ARF ARF. of Glycerol porphyan was is obvious. a common agent for the induction of ARF in vivo and can lead to renal oxidativeResearchers stress, asfound previously many factors reported of [sulfated15]. Therefore, polysaccharides, the protective such effect as molecular on glycerol-induced weight, degree ARF ofof sulfation, porphyan and is obvious. type of sugar, that influence their antioxidant activity. The earlier studies in our laboratoryResearchers showed found that manydifferent factors molecular of sulfated weights polysaccharides, of porphyan suchcould as influence molecular the weight, antioxidant degree activityof sulfation, [16]. Lower and type molecular of sugar, weight that influence porphyan their exhibited antioxidant stronger activity. antioxidant The earlier activity studies compared in our withlaboratory native porphyan. showed that In this different paper, molecular we prepared weights oligo of‐porphyran porphyan by could acid hydrolysis influence the and antioxidant evaluated theactivity structure [16]. and Lower effect molecular of oligo weight‐porphyran porphyan on the exhibited glycerol stronger‐induced antioxidant ARF in rats. activity Dexamethasone compared was with usednative in porphyan.the positive In control this paper, group we due prepared to its anti oligo-porphyran‐inflammatory and by acid antioxidant hydrolysis property and evaluated in ARF rats the [6].structure The levels and effectof blood of oligo-porphyran urea nitrogen (BUN), on the serum glycerol-induced creatinine (SCR), ARF in and rats. ions Dexamethasone in the rats’ blood was usedand urinein the were positive investigated. control group The dueaim toof itsthis anti-inflammatory study was to clarify and antioxidantthe structure property and nephroprotective in ARF rats [6]. activityThe levels of oligo of blood‐porphyran urea nitrogen on glycerol (BUN),‐induced serum creatinineacute renal (SCR), failure and in ionsrats. in the rats’ blood and urine were investigated. The aim of this study was to clarify the structure and nephroprotective activity of 2.oligo-porphyran Results on glycerol-induced acute renal failure in rats. 2.1.2. Results The Structure Study of Oligo‐Porphran 2.1.1.2.1. The Preparation, Structure StudyFraction, of Oligo-Porphran and Analysis of Oligo‐Porphyran (OP) 2.1.1.The Preparation, chemical composition Fraction, and of Analysis the oligo of‐porphyran Oligo-Porphyran (OP) used (OP) in this study was shown in Table 1. It contains 71.39% galactose, 7.05% 3,6‐anhydrogalactose, and 18.32% sulfate groups. Its average The chemical composition of the oligo-porphyran (OP) used in this study was shown in Table1. molecular weight was 1431 Da. This oligosaccharide was mainly composed of sulfated galactan with It contains 71.39% galactose, 7.05% 3,6-anhydrogalactose, and 18.32% sulfate groups. Its average the degree of polymerization ranging from 1 to 8. molecular weight was 1431 Da. This oligosaccharide was mainly composed of sulfated galactan with the degree of polymerization ranging from 1 to 8. Table 1. The chemical analysis of OP. Mw SulfateTable 1. GroupThe chemical Galactose analysis of OP.3,6‐anhydrogalactose Sample (Kda) (%) (%) (%) SampleOP Mw (Kda)1.43 16.90 Sulfate ± 0.51 Group (%)59.93 ± Galactose 1.44 (%)6.45 3,6-anhydrogalactose ± 0.17 (%) OP 1.43 16.90 ± 0.51 59.93 ± 1.44 6.45 ± 0.17 The eluting profile of chromatography of OP was shown in Figure 1. Three fractions were obtained:The F1, eluting F2, and profile F3 from of chromatography 0 to 0.3 M NaCl of elutions OP was from shown column in Figure chromatography,1. Three fractions and the were F4 fractionobtained: was F1, obtained F2, and from F3 from a 0.5 0 toM 0.3NaCl M elution. NaCl elutions The sulfate from group column of chromatography, F1–F4 was 16.54%, and 16.06%, the F4 18.98%,fraction and was 23.18%, obtained respectively. from a 0.5 M NaCl elution. The sulfate group of F1–F4 was 16.54%, 16.06%, 18.98%, and 23.18%, respectively. 2 0.6 Water 0.5 1.5 0.4 F1 F4 1 F2 F3 0.3 0.2 0.5 0.1 NaCl（mol/L） Absorbance 0 0 0 50 100 150 200 250 Elution volume(mL) Figure 1. Chromatography of eluted OP on DEAE-sepharose CL-6B chromatography. Figure 1. Chromatography of eluted OP on DEAE‐sepharose CL‐6B chromatography. Mar. Drugs 2017, 15, 135 3 of 13 Mar. Drugs 2017, 15, 135 3 of 13 2.1.2. Structure of Oligo-PorphyranOligo‐Porphyran (OP) The degree of polymerization (DP) of OP and its fractions fractions F1–F4 F1–F4 was was tested tested by by HPLC HPLC (Figure (Figure 22).). The number of sulfate groups and DPs of OP increased from F1 to F4. The sulfate group numbers of F1~F4 were were 1, 2, 3, and >3, respectively, respectively, while the DPs of their main components were were 2–4, 4–6, 6–8, and 7–13, respectively. Figure 2. Cont. Mar. Drugs 2017, 15, 135 4 of 13 Mar. Drugs 2017, 15, 135 4 of 13 FigureFigure 2. 2. TheThe degreedegree ofof polymerizationpolymerization of of OP OP and and its its fractions fractions tested tested by by HPLC. HPLC. WeWe studied the the molecular molecular weight weight distribution distribution and and structure structure of F1–F4 of F1–F4 using ESI using‐TOF ESI-TOF-MS‐MS (Figure (Figure3). From3). the From MS‐spectrum the MS-spectrum of F1, we found of F1, a wedistribution found a of distribution singly‐charged of singly-chargedions corresponding ions to − − corresponding[Galn‐SO3H‐H] to (n [Gal = 2–6).n-SO There3H-H] were(n =less 2–6). intensive There weresignals, less which intensive were signals, found to which be [3,6 were‐AG found‐Galn‐ − − toSO be3H [3,6-AG-Gal‐H] (n = 3–4).n-SO Analysis3H-H] of(n the= 3–4). spectrum Analysis of F2 of found the spectrum a distribution of F2 foundof doubly a distribution‐charged ions of 2− 2− doubly-chargedcorresponding to ions [Gal correspondingn‐(SO3H)2‐2H] to (n [Gal = 3–7),n-(SO which3H)2 -2H]means (F2n =was 3–7), mainly which made means of disulfate F2 was mainly‐oligo‐ madegalactan.
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