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Reverse cholesterol transport (RCT) is generally defined as cholesterol efflux from peripheral cells to plasma HDL uptaked by hepatocytes for utilization, direct secretion into bile and feces disposal [1, 2]. Therefore, the intact HDL functionalities have been believed to be atheroprotective in atherosclerosis development [3]. Cholesteryl ester transfer protein (CETP) facilitates removal of cholesterol ester from plasma HDL in exchange for triglycerides from low-density lipoproteins or very low-density lipoproteins (LDL or VLDL) [4, 5]. Since wild C57BL/6 J mouse lacks CETP gene necessary for simulating human lipid profiles [6], human CETP transgenic heterozygous mice with a C57BL/6J background were used in the present study.
Both animal and human studies have demonstrated that cigarette smoke (CS) exposure significantly increased levels of plasma total cholesterol (TC), total triglyceride (TG), LDL-cholesterol (LDL-C), but decreased the level of HDL-Cholesterol (HDL-C) [7–9]. A few in vitro studies revealed that CS exposure promoted the modification of lysine amino residue on HDL which would thus lose the functionality to stimulate cholesterol efflux from macrophages [10, 11]. On the other hand, our previous studies demonstrated that H2-rich water or H2-saturated saline decreased aortic atherosclerosis, improved HDL functionalities, and reduced the oxidative stress in animal models or metabolic syndrome volunteers [12–14]. Based on these findings, we proposed that CS exposure in vivo impairs HDL functionalities or RCT pathway in CETP transgenic mice, and that the impairment by CS exposure could be minimized by treatment of H2-saturated saline.
Acetylated low density lipoprotein particles (ac-LDL) were prepared from 48 mL of fresh blood from a healthy volunteer by sequential ultracentrifugation [15]. [3H]-labeled-cholesterol was purchased from PerkinElmer (Waltham, MA, USA). Enzymatic assay kits for plasma lipid determinations were purchased from BioSino (Beijing, China). Kit for measuring formation of thiobarbituric acid reactive substances (TBARS) was from Jiancheng Biochemistry (Najing, China). All antibodies were purchased from Abcam (Cambridge, MA, USA). Commercial Taishan cigarettes (11 mg of tar,1.1 mg of nicotine,12 mg of carbon monoxide, Shandong, China) are used in the present study.
Mice of human CETP transgenic strain with a C57BL/6J background were presented by Dr. Xiancheng Jiang (Department of Anatomy and Cell Biology, SUNY Downstate Medical Center). All CETP transgenic mice were offspring littermates of CETP heterozygous mice. Seventy-two male CETP transgenic mice, 10 weeks old, fed a chow diet (Keaoxieli Co. LTD, Beijing, China) and water ad libitum, were housed in a temperature and humidity controlled room with a 12/12 h light–dark cycle. Mice were exposed to either room air or CS at five cigarettes/d and 5 d/wk for 12 weeks. During the last four weeks the mice were intraperitoneally injected with H2-saturated saline or vehicle (saline) once daily. All animal experiments were conducted in accordance with the Guidelines for Care and Use of Laboratory Animals of Taishan Medical University, and this study was approved by the Laboratory Animals’ Ethical Committee of Taishan Medical University.
The animals were randomly divided into the control group, the H2 group (H2-saturated saline treated, 5 mL/kg/d), the CS group (CS exposed) and the H2 + CS group (H2-saturated saline treated plus CS exposed) (n = 18). In addition, a group of eight C57BL/6J mice were added in the experiment of plasma lipid determination to verify the phenotype of CETP transgenic mice.
Cages for CS exposure were re-designed according to Escolar et al. [16]. Briefly, the cages (42.5 × 26.6 × 19 cm) were equipped with a disposable filter cover having 15 10-mm holes that enabled inside air to be flown out of the cages and thus to be continuously renewed. CS was produced by cigarette burning and introduced into the chamber with airflow generated by a 50 mL medical syringe manipulated by a researcher, at a rate of 125 mL/min. Five cigarettes were smoked one by one within 20 min. A rodent ventilator (Ugo Basile, Shanghai, China) was used to provide fresh room air for dilution (1:8) of smoke stream.
H2 was produced with a self-designed apparatus and immediately dissolved into normal sterile saline to supersaturated concentration for 2 h under high pressure (0.6 MPa). H2-saturated saline, stored under atmospheric pressure and 4 °C, was freshly prepared every 3 days to ensure a constant H2 concentration of not less than 0.6 mM.
Briefly, as described by Yu et al. [17], Raw264.7 cells were incubated with [3H]-cholesterol (5 μCi/mL) and ac-LDL (100 μg/mL) for 48 h, and were then harvested at 1.0 × 106 cells/mL for intraperitoneal injection into mice. The ratio of the intracellular [3H]-cholesterol radioactivity to the total [3H]-cholesterol radioactivity was more than 95 %, which indicated the harvested macrophages had already uptaken 95 % of the total [3H]-cholesterol and thus were in good condition.
After CS exposure or H2-saturated saline treatment, nine mice from each group were injected intraperitoneally with 0.5 mL of [3H]-cholesterol-laden macrophage suspension. At 0, 6, 12 and 24 h after injection, blood was collected from the retro-orbital sinus with heparinized capillary tubes without dietary exposure for 12 h. The mice were then anesthetized with aether and sacrificed at 24 h after injection. Samples of bile, liver, and feces were collected, measured or weighed, and stored at −80 °C for radioactivity determination (n =9). Plasma samples were isolated from blood by centrifugation for liquid scintillation counting.
The cholesterol efflux experiments were performed according to Smith et al. [18]. HDL was isolated from each group of mice by sequential ultracentrifugation. Raw264.7 macrophages at 50 % confluence were co-cultured with acLDL (100 μg/mL) containing [3H]-cholesterol (1 μCi/mL) in RGGB (RPMI 1640 supplemented with 50 mM glucose, 2 mM glutamine and 0.1 % BSA) for 30 min. The macrophages were washed with PBS containing 0.1 % BSA, equilibrated with RGGB for 24 h, and cultured for 16 h in the presence of 300 μM dibutyryl cyclic AMP (dBcAMP). The culture medium was then replaced with RGGB containing 200 μg/mL of HDL isolated from each group of mice. The medium supernatants were collected for radioactivity determination after 12 h of incubation. The macrophages were washed and dissolved in 0.4 mL of 0.1 M sodium hydroxide,