High-Density Lipoprotein (HDL) Inhibits Serum Amyloid A (SAA)-Induced Vascular and Renal Dysfunctions in Apolipoprotein E-Deficient Mice
Abstract
:1. Introduction
2. Results
2.1. Evidence that HDL Inhibits the Pro-Atherogenic Activity of SAA
2.1.1. HDL Pretreatment Inhibits SAA-Induced Aortic Lesions
2.1.2. HDL Pretreatment Mitigates SAA-Induced Pro-Atherogenic Changes to the Vasculature
2.2. HDL Pretreatment Inhibits Oxidative Lipid Damage in the Vasculature
2.3. Analyses of Heart Tissues
2.3.1. HDL Pretreatment Mitigates SAA-Induced Pro-Atherogenic Cardiac Vasculature
2.3.2. Inflammatory Cytokines Expression
2.4. Kidney Function Studies
2.4.1. SAA Stimulates Renal Vascular Endothelium Dysfunction and HDL Mitigates These Changes
2.4.2. HDL Pretreatment Protects Renal Tissues from SAA-Induced Acute Injury
2.4.3. Human HDL Modulates SAA-Mediated Oxidative Stress in Renal Tissues
2.4.4. Pretreatment with HDL Inhibits SAA Induced Pro-Inflammatory Cytokine Stimulation
2.4.5. SAA Stimulates p-38/MAPK Activation
3. Discussion
Study Limitations
- We used a common genetically modified mouse model to assess atherosclerosis and accept that the shortcomings of this model, as identified in the statement, are a general limitation of this experimental model.
- Further validating experiments using nonrodent-based animal models (such as rabbits, pigs, and nonhuman primates) are absolutely required before the conclusions drawn from this study can be translated to human conditions where elevated SAA levels may impact on vascular and renal function.
- In the experimental design, we refrained from using a high-fat diet to accelerate atherosclerosis as the hypothesis being tested was that SAA itself plays a role in promoting pro-atherogenic factors that accelerate atherosclerosis and so a high-fat diet would interfere with this assessment.
- We used a reputable supplier of ApoE-/- mice in Australia (Animal Resources Centre (Perth, Western Australia)) that supply a range of mice for research purposes, and mice were contained in the same environment within the animal facility with the access to the same chow and water supply.
- Mice (8 weeks old) were transported to a local site for husbandry, allowed to acclimate, and then were randomly divided into four groups without internal bias.
- Data obtained using (1) analytical and (2) imaging techniques reported in this study were repeated using the same tissues at the same time for all of the treatment cohorts to gain a valid and rigorous comparison between vehicle, LPS, SAA, and HDL-intervention cohorts.
- We reported how often a given experiment was repeated to substantiate the outcome, and this was established using the nominated statistical tests with appropriate corrections.
4. Experimental Section
4.1. Materials
4.2. Methods
4.2.1. Isolation of Human HDL
4.2.2. Animals
4.2.3. Experimental Groups
- (1)
- Vehicle control group: Mice received 100 µL of sterile saline via intraperitoneal (i.p.) injection route every third day for 14 days.
- (2)
- LPS group: Mice received LPS (equivalent to 25 pg LPS/kg) via i.p. injection route every third day over 14 days. This second (positive) control was included at a slightly higher concentration of LPS determined in the SAA preparation to rule out whether biological effects induced by SAA could be attributed to the LPS contaminant in the SAA protein preparation.
- (3)
- SAA group: Mice received 100 µL of SAA (stock solution 120 μg SAA/mL, total SAA 10 μg/kg mouse/injection) via i.p. injection route every third day for 14 days.
- (4)
- HDL group: Mice designated to receive HDL supplements were pre-injected with 100 μL of stock purified human high-density lipoprotein (HDL) (freshly isolated human HDL preparations were diluted in sterile PBS to yield a stock concentration of 1 mg HDL protein/mL, total 100 μg HDL protein/per kg mouse) every third day via tail vein injection for 14 days prior to treatment with SAA (as described above in group 3). In summary, mice received HDL for two weeks prior to the administration of SAA for the ensuing two weeks.
4.2.4. Urine and Blood
4.2.5. Collection of Aorta, Heart, and Kidney Specimens
4.2.6. Gene Expression Studies
4.2.7. Analysis of Inflammatory Proteins and a Biomarker of Kidney Injury with ELISA
4.2.8. Assessment of Renal 3-Chloro-Tyrosine/Tyrosine Ratio
4.2.9. Assessment of Aortic Lipid Oxidation
4.2.10. Cyclic Guanosine Monophosphate (cGMP) Assessment
4.2.11. Immunohistochemistry (IHC) Studies
4.2.12. Immunofluorescence (IF) Studies
4.2.13. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Gene | Forward | Reverse | NCIB Accession Number |
---|---|---|---|
TNF | 5′-ATGAGCACTGAAAGCATGATCC-3′ | 5′-GAGGGCTGATTAGAGAGAGGTC-3′ | NM_000594.4 |
NFκB | 5′-CTGGAAGCACGAATGACAGA-3′ | 5′-TGAGGTCCATCTCCTTGGTC-3′ | NM_001319226.2 |
VCAM-1 | 5’CCACAAGGCTACATGAGGGT-3’ | 5’-CAGTGTGGATGTAGCCCCTT-3’ | NM_012889.1 |
VEGF | 5′-TTTCTTGCGCTTTCGTTTTT-3′ | 5′-CCCACTGAGGAGTCCAACAT-3′ | NM_001025366.3 |
ACTB | 5′-CATGTACGTTGCTATCCAGG-3′ | 5′-CTCCTTAATGTCACGCACGAT-3′ | NM_001101.5 |
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Cai, X.; Ahmad, G.; Hossain, F.; Liu, Y.; Wang, X.; Dennis, J.; Freedman, B.; Witting, P.K. High-Density Lipoprotein (HDL) Inhibits Serum Amyloid A (SAA)-Induced Vascular and Renal Dysfunctions in Apolipoprotein E-Deficient Mice. Int. J. Mol. Sci. 2020, 21, 1316. https://doi.org/10.3390/ijms21041316
Cai X, Ahmad G, Hossain F, Liu Y, Wang X, Dennis J, Freedman B, Witting PK. High-Density Lipoprotein (HDL) Inhibits Serum Amyloid A (SAA)-Induced Vascular and Renal Dysfunctions in Apolipoprotein E-Deficient Mice. International Journal of Molecular Sciences. 2020; 21(4):1316. https://doi.org/10.3390/ijms21041316
Chicago/Turabian StyleCai, Xiaoping, Gulfam Ahmad, Farjaneh Hossain, Yuyang Liu, XiaoSuo Wang, Joanne Dennis, Ben Freedman, and Paul K. Witting. 2020. "High-Density Lipoprotein (HDL) Inhibits Serum Amyloid A (SAA)-Induced Vascular and Renal Dysfunctions in Apolipoprotein E-Deficient Mice" International Journal of Molecular Sciences 21, no. 4: 1316. https://doi.org/10.3390/ijms21041316