Atherogenic scavenger receptor modulation in the tubulointerstitium in response to chronic renal injury.

Oxidized low-density lipoproteins (oxLDL) and their scavenger receptor (SR) binding partners play a central role in atherosclerosis and by analogy may play a role in chronic kidney disease pathogenesis. The present study was designed to investigate in C57BL/6 mice the effects of hypercholesterolemia on renal injury severity and oxLDL generation after unilateral ureteral obstruction (UUO). The expression profiles of CD36, SR class AI/II (SR-A), lectin-like receptor for oxidized low-density lipoprotein-1 (Lox-1), and SR that binds phosphatidylserine and oxLDL (SR-PSOX/CXCL16) were examined. Four experimental groups were studied: sham and UUO male mice on either a high-fat Western diet or a control diet. Significantly more oxLDL accumulated in the tubulointerstitium of hypercholesterolemic mice compared with normocholesterolemic mice after 14 days of UUO (P < 0.01). Total kidney collagen was significantly higher in the obstructed kidneys of hypercholesterolemic mice compared with normocholesterolemic mice on day 14 (P < 0.01). After 14 days of obstruction, the number of interstitial F4/80+ macrophages and NF-kappaB activation increased in hypercholesterolemic mice compared with normocholesterolemic mice (P < 0.01). In normal kidneys, CD36, SR-A, Lox-1, and CXCL16 were primarily localized to renal tubular epithelia. After ureteral obstruction, CD36 increased at day 7; SR-A and Lox-1 progressively decreased in a time-dependent manner; and CXCL16 increased significantly with the onset of obstruction (P < 0.01). Strong tubular expression suggests that in addition to inflammatory interstitial cells, renal tubular scavenger receptors may help to orchestrate the inflammatory and fibrogenic pathways that are activated by oxLDL.

[1]  T. Kodama,et al.  Macrophage Scavenger Receptor-A–Deficient Mice Are Resistant Against Diabetic Nephropathy Through Amelioration of Microinflammation , 2007, Diabetes.

[2]  I. Charo,et al.  Targeted Disruption of the Scavenger Receptor and Chemokine CXCL16 Accelerates Atherosclerosis , 2006, Circulation.

[3]  S. Chua,et al.  Plasminogen Activator Inhibitor-1 Deficiency Has Renal Benefits but Some Adverse Systemic Consequences in Diabetic Mice , 2006, Nephron Experimental Nephrology.

[4]  K. Davies,et al.  Identification and Characterization of Murine SCARA5, a Novel Class A Scavenger Receptor That Is Expressed by Populations of Epithelial Cells* , 2006, Journal of Biological Chemistry.

[5]  J. Odeberg,et al.  Alternative promoter usage of the membrane glycoprotein CD36 , 2006, BMC Molecular Biology.

[6]  S. Yonehara,et al.  The Membrane-Bound Chemokine CXCL16 Expressed on Follicle-Associated Epithelium and M Cells Mediates Lympho-Epithelial Interaction in GALT1 , 2006, The Journal of Immunology.

[7]  L. Lerman,et al.  Pathways of Renal Fibrosis and Modulation of Matrix Turnover in Experimental Hypercholesterolemia , 2005, Hypertension.

[8]  A. Holian,et al.  Scavenger receptor class A type I/II (CD204) null mice fail to develop fibrosis following silica exposure. , 2005, American journal of physiology. Lung cellular and molecular physiology.

[9]  Roger E Bumgarner,et al.  Multifunctionality of PAI-1 in fibrogenesis: evidence from obstructive nephropathy in PAI-1-overexpressing mice. , 2005, Kidney international.

[10]  I. Ohki,et al.  Crystal structure of human lectin-like, oxidized low-density lipoprotein receptor 1 ligand binding domain and its ligand recognition mode to OxLDL. , 2005, Structure.

[11]  N. Davidson,et al.  CD36 deficiency impairs intestinal lipid secretion and clearance of chylomicrons from the blood. , 2005, The Journal of clinical investigation.

[12]  K. Hirata,et al.  Oxidized Phosphatidylcholine in AlveolarMacrophages in Idiopathic Interstitial Pneumonias , 2005, Lung.

[13]  K. Suszták,et al.  Multiple Metabolic Hits Converge on CD36 as Novel Mediator of Tubular Epithelial Apoptosis in Diabetic Nephropathy , 2005, PLoS medicine.

[14]  N. Kobayashi,et al.  Cardioprotective mechanisms of Rho-kinase inhibition associated with eNOS and oxidative stress-LOX-1 pathway in Dahl salt-sensitive hypertensive rats , 2005, Journal of hypertension.

[15]  S. Pizzo,et al.  SREC-I, a Type F Scavenger Receptor, Is an Endocytic Receptor for Calreticulin* , 2004, Journal of Biological Chemistry.

[16]  S. Gordon,et al.  The Class A Macrophage Scavenger Receptor Attenuates CXC Chemokine Production and the Early Infiltration of Neutrophils in Sterile Peritonitis1 , 2004, The Journal of Immunology.

[17]  L. Kobzik,et al.  Scavenger receptor A mediates H2O2 production and suppression of IL‐12 release in murine macrophages , 2004, Journal of leukocyte biology.

[18]  S. Gordon,et al.  Activation of murine macrophages by Neisseria meningitidis and IFN‐γ in vitro: distinct roles of class A scavenger and Toll‐like pattern recognition receptors in selective modulation of surface phenotype , 2004, Journal of leukocyte biology.

[19]  K. Tryggvason,et al.  The Scavenger Receptor MARCO Is Required for Lung Defense against Pneumococcal Pneumonia and Inhaled Particles , 2004, The Journal of experimental medicine.

[20]  E. Ritman,et al.  Antioxidant intervention prevents renal neovascularization in hypercholesterolemic pigs. , 2004, Journal of the American Society of Nephrology : JASN.

[21]  M. Goligorsky,et al.  Upregulation of lectin-like oxidized low-density lipoprotein receptor-1 (LOX-1) in endothelial cells by nitric oxide deficiency. , 2004, American journal of physiology. Renal physiology.

[22]  T. Kita,et al.  Chemokines Generally Exhibit Scavenger Receptor Activity through Their Receptor-binding Domain* , 2004, Journal of Biological Chemistry.

[23]  P. Dempsey,et al.  A Disintegrin and Metalloproteinase 10-Mediated Cleavage and Shedding Regulates the Cell Surface Expression of CXC Chemokine Ligand 16 , 2004, The Journal of Immunology.

[24]  T. Kita,et al.  Cutting Edge: SR-PSOX/CXC Chemokine Ligand 16 Mediates Bacterial Phagocytosis by APCs Through its Chemokine Domain1 , 2003, The Journal of Immunology.

[25]  De-Pei Liu,et al.  Excessive expression of the scavenger receptor class A type I can significantly affect the serum lipids. , 2003, Sheng wu hua xue yu sheng wu wu li xue bao Acta biochimica et biophysica Sinica.

[26]  K. Moore,et al.  Scavenger Receptors Class A-I/II and CD36 Are the Principal Receptors Responsible for the Uptake of Modified Low Density Lipoprotein Leading to Lipid Loading in Macrophages* , 2002, The Journal of Biological Chemistry.

[27]  K. Moore,et al.  A CD36-initiated Signaling Cascade Mediates Inflammatory Effects of β-Amyloid* , 2002, The Journal of Biological Chemistry.

[28]  Alan Daugherty,et al.  Macrophage-specific expression of class A scavenger receptors in LDL receptor−/− mice decreases atherosclerosis and changes spleen morphology DOI 10.1194/jlr.M200116-JLR200 , 2002, Journal of Lipid Research.

[29]  H. Robenek,et al.  Expression of the novel scavenger receptor SR-PSOX in cultured aortic smooth muscle cells and umbilical endothelial cells. , 2002, Arteriosclerosis, thrombosis, and vascular biology.

[30]  Masashi Komeda,et al.  Expression of SR-PSOX, a Novel Cell-Surface Scavenger Receptor for Phosphatidylserine and Oxidized LDL in Human Atherosclerotic Lesions , 2001, Arteriosclerosis, thrombosis, and vascular biology.

[31]  R. Silverstein,et al.  CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. , 2001, The Journal of clinical investigation.

[32]  D. Paulnock,et al.  Signaling pathways initiated in macrophages after engagement of type A scavenger receptors , 2001, Journal of leukocyte biology.

[33]  E. van Marck,et al.  Oxidative modification of low-density lipoproteins and the outcome of renal allografts at 1 1/2 years. , 2001, Kidney international.

[34]  E. Kunkel,et al.  Bonzo/CXCR6 expression defines type 1-polarized T-cell subsets with extralymphoid tissue homing potential. , 2001, The Journal of clinical investigation.

[35]  N. Kuemmerle,et al.  α-Tocopherol modulates lipoprotein cytotoxicity in obstructive nephropathy , 2000, Pediatric Nephrology.

[36]  R. E. Pitas,et al.  Class A Scavenger Receptor Up-regulation in Smooth Muscle Cells by Oxidized Low Density Lipoprotein* , 2000, The Journal of Biological Chemistry.

[37]  Jihong Han,et al.  CD36 in Atherosclerosis: The Role of a Class B Macrophage Scavenger Receptor , 2000 .

[38]  T. Sawamura,et al.  Oxidized Low Density Lipoprotein (ox-LDL) Binding to ox-LDL Receptor-1 in Endothelial Cells Induces the Activation of NF-κB through an Increased Production of Intracellular Reactive Oxygen Species* , 2000, The Journal of Biological Chemistry.

[39]  S. Hazen,et al.  Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. , 2000, The Journal of clinical investigation.

[40]  S. Hazen,et al.  The Oxidation of Lipoproteins by Monocytes-Macrophages , 1999, The Journal of Biological Chemistry.

[41]  Z. Varghese,et al.  Human mesangial cells express inducible macrophage scavenger receptor. , 1999, Kidney international.

[42]  M. Pfeffer,et al.  Controlling the epidemic of cardiovascular disease in chronic renal disease: what do we know? What do we need to learn? Where do we go from here? National Kidney Foundation Task Force on Cardiovascular Disease. , 1998, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[43]  K. Nakashima,et al.  Apolipoprotein E Polymorphism in Patients with Alzheimer’s Disease, Vascular Dementia and Ischemic Cerebrovascular Disease , 1998, Dementia and Geriatric Cognitive Disorders.

[44]  T. Kodama,et al.  Role of macrophage scavenger receptors in diet-induced atherosclerosis in mice. , 1998, Laboratory investigation; a journal of technical methods and pathology.

[45]  A. Eddy,et al.  Failure of antioxidant therapy to attenuate interstitial disease in rats with reversible nephrotic syndrome. , 1998, Journal of the American Society of Nephrology : JASN.

[46]  S. Parthasarathy,et al.  Interaction of Interceed oxidized regenerated cellulose with macrophages: a potential mechanism by which Interceed may prevent adhesions. , 1997, American journal of obstetrics and gynecology.

[47]  Yukiko Kurihara,et al.  A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection , 1997, Nature.

[48]  R. Silverstein,et al.  Regulation of monocyte CD36 and thrombospondin-1 expression by soluble mediators. , 1996, Arteriosclerosis, thrombosis, and vascular biology.

[49]  L. Yesner,et al.  Regulated expression of CD36 during monocyte-to-macrophage differentiation: potential role of CD36 in foam cell formation. , 1996, Blood.

[50]  S. Ryeom,et al.  CD36 participates in the phagocytosis of rod outer segments by retinal pigment epithelium. , 1996, Journal of cell science.

[51]  B. Paigen,et al.  Comparison of atherosclerotic lesions and HDL-lipid levels in male, female, and testosterone-treated female mice from strains C57BL/6, BALB/c, and C3H. , 1987, Atherosclerosis.

[52]  K. Hirata,et al.  Oxidized phosphatidylcholine in alveolar macrophages in idiopathic interstitial pneumonias. , 2005, Lung.

[53]  Maristela L Onozato,et al.  LOX-1, an oxidized low-density lipoprotein receptor, was upregulated in the kidneys of chronic renal failure rats. , 2003, Hypertension research : official journal of the Japanese Society of Hypertension.

[54]  K. Moore,et al.  A CD36-initiated signaling cascade mediates inflammatory effects of beta-amyloid. , 2002, The Journal of biological chemistry.

[55]  N. Kuemmerle,et al.  Alpha-tocopherol modulates lipoprotein cytotoxicity in obstructive nephropathy. , 2000, Pediatric nephrology.

[56]  K. Matsumoto,et al.  Oxidized LDL-induced NF-kappa B activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[57]  Robert Lipsky,et al.  The carboxyl-terminal cytoplasmic domain of CD36 is required for oxidized low-density lipoprotein modulation of NF-kappaB activity by tumor necrosis factor-alpha. , 1997, Receptors & signal transduction.