CXCR4 promotes renal tubular cell survival in male diabetic rats: Implications for ligand inactivation in the human kidney

Endocrinology (United States)

Volumn 156, Issue 3, 2015, Pages 1121-1132

  Siddiqi, Ferhan S ^a,b   Chen, Li Hao ^a,b   Advani, Suzanne L ^a,b   Thai, Kerri ^a,b   Batchu, Sri N ^a,b   Alghamdi, Tamadher A ^a,b   White, Kathryn E ^c   Sood, Manish M ^d   Gibson, Ian W ^e   Connelly, Kim A ^a,b   Marsden, Philip A ^a,b   Advani, Andrew ^a,b,f  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^e UNIVERSITY OF MANITOBA   (Canada)

^f ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; GELATINASE B; PLERIXAFOR; PROTEIN BCL 2; PROTEIN KINASE B; PROTEINASE; SERINE; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN; CHEMOKINE RECEPTOR CXCR; CMKOR1 PROTEIN, RAT; CXCL12 PROTEIN, RAT; CXCR4 PROTEIN, HUMAN; CXCR4 PROTEIN, RAT; HETEROCYCLIC COMPOUND;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DIABETIC NEPHROPATHY; FEMALE; GENE EXPRESSION; GLOMERULUS FILTRATION RATE; HUMAN; HUMAN CELL; KIDNEY TUBULE CELL; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; UPREGULATION; ANIMAL; CYTOLOGY; EPITHELIUM CELL; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION REGULATION; GENETICS; KIDNEY TUBULE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ALBUMINURIA; ANIMALS; CELL SURVIVAL; CHEMOKINE CXCL12; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HETEROCYCLIC COMPOUNDS; HUMANS; KIDNEY TUBULES; MALE; MATRIX METALLOPROTEINASE 9; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CXCR; RECEPTORS, CXCR4;

EID: 84923924174     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1650     Document Type: Article

References (55)

1. Taft JL, Nolan CJ, Yeung SP, Hewitson TD, Martin FI. Clinical and histological correlations of decline in renal function in diabetic patients with proteinuria. Diabetes. 1994;43(8):1046-1051.
2. Tojo A, Onozato ML, Ha H, et al. Reduced albumin reabsorption in the proximal tubule of early-stage diabetic rats. Histochem Cell Biol. 2001;116(3):269-276.
3. Takabatake Y, Sugiyama T, Kohara H, et al. The CXCL12 (SDF- 1)/CXCR4 axis is essential for the development of renal vasculature. J Am Soc Nephrol. 2009;20(8):1714-1723.
4. Chen LH, Advani SL, Thai K, et al. SDF-1/CXCR4 signaling preserves microvascular integrity and renal function in chronic kidney disease. PloS One. 2014;9(3):e92227.
5. Ding M, Cui S, Li C, et al. Loss of the tumor suppressor Vhlh leads to upregulation of Cxcr4 and rapidly progressive glomerulonephritis in mice. Nat Med. 2006;12(9):1081-1087.
6. Ueland J, Yuan A, Marlier A, Gallagher AR, Karihaloo A. A novel role for the chemokine receptor Cxcr4 in kidney morphogenesis: An in vitro study. Dev Dyn. 2009;238(5):1083-1091.
7. Wehler TC, Graf C, Biesterfeld S, et al. Strong expression of chemokine receptor CXCR4 by renal cell carcinoma correlates with advanced disease. J Oncol. 2008;2008:626340.
8. Neusser MA, Lindenmeyer MT, Moll AG, et al. Human nephrosclerosis triggers a hypoxia-related glomerulopathy. Am J Pathol. 2010; 176(2):594-607.
9. Gilbert RE, Huang Q, Thai K, et al. Histone deacetylase inhibition attenuates diabetes-associated kidney growth: Potential role for epigenetic modification of the epidermal growth factor receptor. Kidney Int. 2011;79:1312-1321.
10. Fricker SP, Anastassov V, Cox J, et al. Characterization of the molecular pharmacology of AMD3100: A specific antagonist of the G-protein coupled chemokine receptor, CXCR4. Biochem Pharmacol. 2006;72(5):588-596.
11. Advani A, Kelly DJ, Advani SL, et al. Role of VEGF in maintaining renal structure and function under normotensive and hypertensive conditions. Proc Natl Acad Sci U S A. 2007;104(36):14448-14453.
12. Advani A, Gilbert RE, Thai K, et al. Expression, localization, and function of the thioredoxin system in diabetic nephropathy. J Am Soc Nephrol. 2009;20(4):730-741.
13. Advani A, Connelly KA, Yuen DA, et al. Fluorescent microangiography is a novel and widely applicable technique for delineating the renal microvasculature. PloS One. 2011;6(10):e24695.
14. Advani A, Huang Q, Thai K, et al. Long-term administration of the histone deacetylase inhibitor vorinostat attenuates renal injury in experimental diabetes through an endothelial nitric oxide synthasedependent mechanism. Am J Pathol. 2011;178(5):2205-2214.
15. Yuen DA, Stead BE, Zhang Y, et al. eNOS deficiency predisposes podocytes to injury in diabetes. J Am Soc Nephrol. 2012;23(11):1810-1823.
16. Advani A, Kelly DJ, Cox AJ, et al. The (Pro)renin receptor: Sitespecific and functional linkage to the vacuolar H+-ATPase in the kidney. Hypertension. 2009;54(2):261-269.
17. Advani A, Wiggins KJ, Cox AJ, Zhang Y, Gilbert RE, Kelly DJ. Inhibition of the epidermal growth factor receptor preserves podocytes and attenuates albuminuria in experimental diabetic nephropathy. Nephrology (Carlton). 2011;16(6):573-581.
18. Saleem MA, O'Hare MJ, Reiser J, et al. A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J Am Soc Nephrol. 2002;13(3):630-638.
19. Petruzziello-Pellegrini TN, Yuen DA, Page AV, et al. The CXCR4/CXCR7/SDF-1 pathway contributes to the pathogenesis of Shiga toxin-associated hemolytic uremic syndrome in humans and mice. J Clin Invest. 2012;122(2):759-776.
20. Cao J, Wang L, Du ZJ, et al. Recruitment of exogenous mesenchymal stem cells in mandibular distraction osteogenesis by the stromal cell-derived factor-1/chemokine receptor-4 pathway in rats. Br J Oral Maxillofac Surg. 2013;51(8):937-941.
21. Wojcechowskyj JA, Lee JY, Seeholzer SH, Doms RW. Quantitative phosphoproteomics ofCXCL12(SDF-1) signaling. PloS One. 2011; 6(9):e24918.
22. Sbardella D, Inzitari R, Iavarone F, et al. Enzymatic processing by MMP-2 and MMP-9 of wild-type and mutated mouse β-dystroglycan. IUBMB Life. 2012;64(12):988-994.
23. Isoe T, Makino Y, Mizumoto K, et al. High glucose activates HIF-1-mediated signal transduction in glomerular mesangial cells through a carbohydrate response element binding protein. Kidney Int. 2010;78(1):48-59.
24. Schrijvers BF, DeVriese AS, Vande Voorde J, Rasch R, Lameire NH, Flyvbjerg A. Long-term renal changes in the Goto-Kakizaki rat, a model of lean type 2 diabetes. Nephrol Dial Transplant. 2004;19(5):1092-1097.
25. Cooper ME, Vranes D, Youssef S, et al. Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes. Diabetes. 1999;48(11):2229-2239.
26. Tögel F, Isaac J, Hu Z, Weiss K, Westenfelder C. Renal SDF-1 signals mobilization and homing of CXCR4-positive cells to the kidney after ischemic injury. Kidney Int. 2005;67(5):1772-1784.
27. Gassenmaier M,Chen D, Buchner A, et al. CXCchemokine receptor 4 is essential for maintenance of renal cell carcinoma-initiating cells and predicts metastasis. Stem Cells. 2013;31(8):1467-1476.
28. Dickson LE, Wagner MC, Sandoval RM, Molitoris BA. The proximal tubule and albuminuria: Really! J Am Soc Nephrol. 2014; 25(3):443-453.
29. Woerner BM, Warrington NM, Kung AL, Perry A, Rubin JB. Widespread CXCR4 activation in astrocytomas revealed by phospho-CXCR4-specific antibodies. Cancer Res. 2005;65(24):11392-11399.
30. McQuibban GA, Butler GS, Gong JH, et al. Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1. The J Biol Chem. 2001;276(47):43503-43508.
31. Advani A. Vascular endothelial growth factor and the kidney: Something of the marvellous. Curr Opin Nephrol Hypertens. 2014;23(1):87-92.
32. Naumann U, Cameroni E, Pruenster M, et al. CXCR7 functions as a scavenger forCXCL12andCXCL11. PloS One. 2010;5(2):e9175.
33. Yang E, Zha J, Jockel J, Boise LH, Thompson CB, Korsmeyer SJ. Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell. 1995;80(2):285-291.
34. Cowburn AS, Cadwallader KA, Reed BJ, Farahi N, Chilvers ER. Role of PI3-kinase-dependent Bad phosphorylation and altered transcription in cytokine-mediated neutrophil survival. Blood. 2002;100(7):2607-2616.
35. Vicente-Manzanares M, Rey M, Jones DR, et al. Involvement of phosphatidylinositol 3-kinase in stromal cell-derived factor-1 al-pha-induced lymphocyte polarization and chemotaxis. J Immunol. 1999;163(7):4001-4012.
36. Luo HR, Hattori H, Hossain MA, et al. Akt as a mediator of cell death. Proc Natl Acad Sci U S A. 2003;100(20):11712-11717.
37. Mochizuki T, Asai A, Saito N, et al. Akt protein kinase inhibits non-apoptotic programmed cell death induced by ceramide. J Biol Chem. 2002;277(4):2790-2797.
38. Brezniceanu ML, Liu F, Wei CC, et al. Attenuation of interstitial fibrosis and tubular apoptosis in db/db transgenic mice overexpressing catalase in renal proximal tubular cells. Diabetes. 2008;57(2):451-459.
39. Huang CS, Tang SJ, Chung LY, et al. Galectin-1 upregulates CXCR4 to promote tumor progression and poor outcome in kidney cancer. J Am Soc Nephrol. 2014;25(7)1486-1495.
40. Linkermann A, Green DR. Necroptosis. N Engl J Med. 2014;370(5):455-465.
41. Weinlich R, Oberst A, Dillon CP, et al. Protective roles for caspase-8 and cFLIP in adult homeostasis. Cell Rep. 2013;5(2):340-348.
42. Wharram BL, Goyal M, Wiggins JE, et al. Podocyte depletion causes glomerulosclerosis: Diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene. J Am Soc Nephrol. 2005;16(10):2941-2952.
43. White KE, Bilous RW, Marshall SM, et al. Podocyte number in normotensive type 1 diabetic patients with albuminuria. Diabetes. 2002;51(10):3083-3089.
44. Sayyed SG, Hägele H, Kulkarni OP, et al. Podocytes produce homeostatic chemokine stromal cell-derived factor-1/CXCL12, which contributes to glomerulosclerosis, podocyte loss and albuminuria in a mouse model of type 2 diabetes. Diabetologia. 2009;52(11):2445-2454.
45. de Nigris F, Crudele V, Giovane A, et al. CXCR4/YY1 inhibition impairs VEGF network and angiogenesis during malignancy. Proc Natl Acad Sci U S A. 2010;107(32):14484-14489.
46. Huber BC, Brunner S, Segeth A, et al. Parathyroid hormone is a DPP-IV inhibitor and increases SDF-1-driven homing ofCXCR4(+) stem cells into the ischaemic heart. Cardiovasc Res. 2011;90(3):529-537.
47. Zheng M, Lv LL, Cao YH, et al. Urinary mRNA markers of epi-thelial-mesenchymal transition correlate with progression of diabetic nephropathy. Clin Endocrinol (Oxf). 2012;76(5):657-664.
48. Li SY, Huang PH, Yang AH, et al. Matrix metalloproteinase-9 deficiency attenuates diabetic nephropathy by modulation of podocyte functions and dedifferentiation. Kidney Int. 2014;86(2):358-369.
49. Hohenstein B, Hausknecht B, Boehmer K, Riess R, Brekken RA, Hugo CP. Local VEGF activity but not VEGF expression is tightly regulated during diabetic nephropathy in man. Kidney Int. 2006; 69(9):1654-1661.
50. Kanasaki K, Shi S, Kanasaki M, et al. Linagliptin-mediated DPP-4 inhibition ameliorates kidney fibrosis in streptozotocin-induced diabetic mice by inhibiting endothelial-to-mesenchymal transition in a therapeutic regimen. Diabetes. 2014;63(6):2120-2131.
51. Hocher B, Reichetzeder C, Alter ML. Renal and cardiac effects of DPP4 inhibitors-from preclinical development to clinical research. Kidney Blood Press Res. 2012;36(1):65-84.
52. Loetscher M, Geiser T, O'Reilly T, Zwahlen R, Baggiolini M, Moser B. Cloning of a human seven-transmembrane domain receptor, LESTR, that is highly expressed in leukocytes. J Biol Chem. 1994; 269(1):232-237.
53. Navarro-Gonzalez JF, Mora-Fernandez C. The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol. 2008; 19(3):433-442.
54. Chu PY, Zatta A, Kiriazis H, et al. CXCR4 antagonism attenuates the cardiorenal consequences of mineralocorticoid excess. Circ Heart Fail. 2011;4(5):651-658.
55. Dai S, Yuan F, Mu J, et al. Chronic AMD3100 antagonism of SDF- 1alpha-CXCR4 exacerbates cardiac dysfunction and remodeling after myocardial infarction. J Mol Cell Cardiol. 2010;49(4):587-597.