Podocyte autophagic activity plays a protective role in renal injury and delays the progression of podocytopathies

Journal of Pathology

Volumn 234, Issue 2, 2014, Pages 203-213

  Zeng, Caihong ^a   Fan, Yun ^a   Wu, Junnan ^a   Shi, Shaolin ^a   Chen, Zhaohong ^a   Zhong, Yongzhong ^a   Zhang, Changming ^a   Zen, Ke ^b   Liu, Zhihong ^a  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

Author keywords

Apoptosis; Autophagy; Beclin1; LC3; Podocyte; Rapamycin

Indexed keywords

3 METHYLADENINE; BECLIN 1; CHLOROQUINE; PUROMYCIN AMINONUCLEOSIDE; RAPAMYCIN; LC3;

ADULT; ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL STIMULATION; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; FEMALE; FOCAL GLOMERULOSCLEROSIS; HUMAN; HUMAN TISSUE; KIDNEY BIOPSY; KIDNEY DISEASE; KIDNEY INJURY; MALE; MINIMAL CHANGE DISEASE; NONHUMAN; PODOCYTE; PROTEINURIA; RAT; ACUTE KIDNEY FAILURE; ANIMAL; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; DRUG EFFECT; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; WISTAR RAT;

APOPTOSIS; AUTOPHAGY; BECLIN1; LC3; PODOCYTE; RAPAMYCIN;

ACUTE KIDNEY INJURY; ANIMALS; APOPTOSIS; AUTOPHAGY; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HUMANS; MALE; PODOCYTES; PROTEINURIA; PUROMYCIN AMINONUCLEOSIDE; RATS, WISTAR;

EID: 84907952998     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4382     Document Type: Article

References (51)

1. Pollak MR. Focal segmental glomerulosclerosis: recent advances. Curr Opin Nephrol Hypertens 2008; 17: 138-142.
2. WaldmanM, CrewRJ,ValeriA, et al. Adultminimal-change disease: clinical characteristics, treatment, and outcomes. Clin J Am Soc Nephrol 2007; 2: 445-453.
3. Park CW, Song HC, Shin YS, et al. Urinary soluble HLA class I antigen in patients with minimal change disease: a predictor of steroid response. Nephron 1998; 79: 44-49.
4. Hara M, Yanagihara T, Kihara I. Urinary podocytes in primary focal segmental glomerulosclerosis. Nephron 2001; 89: 342-347.
5. Srivastava T, Garola RE,Whiting JM, et al. Synaptopodin expression in idiopathic nephrotic syndrome of childhood. Kidney Int 2001; 59: 118-125.
6. Barisoni L. Podocyte biology in segmental sclerosis and progressive glomerular injury. Adv Chronic Kidney Dis 2012; 19: 76-83.
7. D'Agati VD. Podocyte injury in focal segmental glomerulosclerosis: lessons from animal models (a play in five acts). Kidney Int 2008; 73: 399-406.
8. Vogelmann SU, Nelson WJ, Myers BD, et al. Urinary excretion of viable podocytes in health and renal disease. Am J Physiol Renal Physiol 2003; 285: F40-F48.
9. Kriz W, LeHir M. Pathways to nephron loss starting from glomerular diseases - insights from animal models. Kidney Int 2005; 67: 404-419.
10. Schwartz MM. The role of podocyte injury in the pathogenesis of focal segmental glomerulosclerosis. Ren Fail 2000; 22: 663-684.
11. D'Agati VD. The spectrum of focal segmental glomerulosclerosis: new insights. Curr Opin Nephrol Hypertens 2008; 17: 271-281.
12. Kim J, Klionsky DJ. Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu Rev Biochem 2000; 69: 303-342.
13. Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature 2008; 451: 1069-1075.
14. Hartleben B, Godel M, Meyer-Schwesinger C, et al. Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice. J Clin Invest 2010; 120: 1084-1096.
15. Kume S, Uzu T, Horiike K, et al. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J Clin Invest 2010; 120: 1043-1055.
16. Sato S, Yanagihara T, Ghazizadeh M, et al. Correlation of autophagy type in podocytes with histopathological diagnosis of IgA nephropathy. Pathobiology 2009; 76: 221-226.
17. Mizushima N, Levine B. Autophagy in mammalian development and differentiation. Nature Cell Biol 2010; 12: 823-830.
18. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6: 463-477.
19. Kang Y-L, Saleem MA, Chan KW, et al. The cytoprotective role of autophagy in puromycin aminonucleoside treated human podocytes. Biochem Biophys Res Commun 2014; 443: 628-634.
20. Wu L, Feng Z, Cui S, et al. Rapamycin upregulates autophagy by inhibiting the mTOR-ULK1 pathway, resulting in reduced podocyte injury. PLoS One 2013; 8: e63799.
21. Asanuma K, Tanida I, Shirato I, et al. MAP-LC3, a promising autophagosomal marker, is processed during the differentiation and recovery of podocytes from PAN nephrosis. FASEB J 2003; 17: 1165-1167.
22. Cinà DP, Onay T, Paltoo A, et al. Inhibition of MTOR disrupts autophagic flux in podocytes. J Am Soc Nephrol 2012; 23: 412-420.
23. Sato S, Kitamura H, Adachi A, et al. Two types of autophagy in the podocytes in renal biopsy specimens: ultrastructural study. J Submicrosc Cytol Pathol 2006; 38: 167-174.
24. Klionsky DJ, Abdalla FC, Abeliovich H, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544.
25. 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: 630-638.
26. Zheng CX, Chen ZH, Zeng CH, et al. Triptolide protects podocytes from puromycin aminonucleoside induced injury in vivo and in vitro. Kidney Int 2008; 74: 596-612.
27. Sheng R, Zhang LS, Han R, et al. Autophagy activation is associated with neuroprotection in a rat model of focal cerebral ischemic preconditioning. Autophagy 2010; 6: 482-494.
28. Zou Z, Wu L, Ding H, et al. MicroRNA-30a sensitizes tumor cells to cis-platinum via suppressing beclin 1-mediated autophagy. J Biol Chem 2012; 287: 4148-4156.
29. Yu Y, Yang L, Zhao M, et al. Targeting microRNA-30a-mediated autophagy enhances imatinib activity against human chronicmyeloid leukemia cells. Leukemia 2012; 26: 1752-1760.
30. Zhu H, Wu H, Liu X, et al. Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells. Autophagy 2009; 5: 816-823.
31. Li LM, Hou DX, Guo YL, et al. Role of microRNA-214-targeting phosphatase and tensin homolog in advanced glycation end product-induced apoptosis delay in monocytes. J Immunol 2011; 186: 2552-2560.
32. Torras J, Herrero-Fresneda I, Gulias O, et al. Rapamycin has dual opposing effects on proteinuric experimental nephropathies: is it a matter of podocyte damage? Nephrol Dial Transplant 2009; 24: 3632-3640.
33. Diekmann F, Rovira J, Carreras J, et al. Mammalian target of rapamycin inhibition halts the progression of proteinuria in a rat model of reduced renal mass. J Am Soc Nephrol 2007; 18: 2653-2660.
34. Lin CW, Zhang H, Li M, et al. Pharmacological promotion of autophagy alleviates steatosis and injury in alcoholic and non-alcoholic fatty liver conditions in mice. J Hepatol 2013; 58: 993-999.
35. Takemoto M, Asker N, Gerhardt H, et al. A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol 2002; 161: 799-805.
36. Cao Y, Klionsky DJ. Physiological functions of Atg6/Beclin 1: a unique autophagy-related protein. Cell Res 2007; 17: 839-849.
37. Srivastava T, Sharma M, Yew KH, et al. LPS and PAN-induced podocyte injury in an in vitro model of minimal change disease: changes in TLR profile. J Cell Commun Signal 2013; 7: 49-60.
38. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140: 313-326.
39. Chen YC, Lo CL, Lin YF, et al. Rapamycin encapsulated in dual-responsive micelles for cancer therapy. Biomaterials 2013; 34: 1115-1127.
40. Chen J, Chen S, Chen Y, et al. Circulating endothelial progenitor cells and cellular membrane microparticles in db/db diabetic mouse: possible implications in cerebral ischemic damage. Am J Physiol Endocrinol Metab 2011; 301: E62-E71.
41. Shimizu S, Kanaseki T, Mizushima N, et al. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nature Cell Biol 2004; 6: 1221-1228.
42. Sasaki K, Tsuno NH, Sunami E, et al. Chloroquine potentiates the anti-cancer effect of 5-fluorouracil on colon cancer cells. BMC Cancer 2010; 10: 370.
43. Maycotte P, Aryal S, Cummings CT, et al. Chloroquine sensitizes breast cancer cells to chemotherapy independent of autophagy. Autophagy 2012; 8: 200-212.
44. Iwamaru A, Kondo Y, Iwado E, et al. Silencing mammalian target of rapamycin signaling by small interfering RNA enhances rapamycin-induced autophagy in malignant glioma cells. Oncogene 2007; 26: 1840-1851.
45. Cao C, Subhawong T, Albert JM, et al. Inhibition of mammalian target of rapamycin or apoptotic pathway induces autophagy and radiosensitizes PTEN null prostate cancer cells. Cancer Res 2006; 66: 10040-10047.
46. Komatsu M, Waguri S, Ueno T, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005; 169: 425-434.
47. Kuma A, Hatano M, Matsui M, et al. The role of autophagy during the early neonatal starvation period. Nature 2004; 432: 1032-1036.
48. Scott RC, Schuldiner O, Neufeld TP. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev Cell 2004; 7: 167-178.
49. Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011; 147: 728-741.
50. Tao Y, Kim J, Schrier RW, et al. Rapamycin markedly slows disease progression in a rat model of polycystic kidney disease. J Am Soc Nephrol 2005; 16: 46-51.
51. Huber TB,Walz G, Kuehn EW. mTOR and rapamycin in the kidney: signaling and therapeutic implications beyond immunosuppression. Kidney Int 2011; 79: 502-511.