Polycystic kidney disease: A case of suppressed autophagy?

Seminars in Nephrology

Volumn 34, Issue 1, 2014, Pages 27-33

  Ravichandran, Kameswaran ^a   Edelstein, Charles L ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Apoptosis; Autophagy; Polycystic kidney

Indexed keywords

POLYCYSTIN 1; RAPAMYCIN;

APOPTOSIS; AUTOPHAGY; DRUG MECHANISM; EUKARYOTIC FLAGELLUM; GENE INACTIVATION; HUMAN; KIDNEY POLYCYSTIC DISEASE; METABOLIC INHIBITION; MISSENSE MUTATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TUMOR GROWTH;

APOPTOSIS; AUTOPHAGY; POLYCYSTIC KIDNEY;

ANIMALS; APOPTOSIS; AUTOPHAGY; CILIA; HUMANS; MICE; POLYCYSTIC KIDNEY DISEASES; PROTEINS; SIGNAL TRANSDUCTION;

EID: 84893406789     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2013.11.005     Document Type: Review

References (68)

1. Tao Y., Kim J., Schrier R.W., Edelstein C.L. Rapamycin markedly slows disease progression in a rat model of polycystic kidney disease (PKD). J Am Soc Nephrol 2005, 16:46-51.
2. Zafar I., Ravichandran K., Belibi F., Doctor R.B., Edelstein C.L. Sirolimus attenuates disease progression in an orthologous mouse model of human autosomal dominant polycystic kidney disease. Kidney Int 2010, 78:754-761.
3. Shillingford J.M., Piontek K.B., Germino G.G., Weimbs T. Rapamycin ameliorates PKD resulting from conditional inactivation of Pkd1. J Am Soc Nephrol 2010, 21:489-497.
4. Huber T.B., Walz G., Kuehn E.W. mTOR and rapamycin in the kidney: signaling and therapeutic implications beyond immunosuppression. Kidney Int 2011, 79:502-511.
5. Walz G., Budde K., Mannaa M., Nurnberger J., Wanner C., Sommerer C., et al. Everolimus in patients with autosomal dominant polycystic kidney disease. N Engl J Med 2010, 363:830-840.
6. Serra A.L., Poster D., Kistler A.D., Krauer F., Raina S., Young J., et al. Sirolimus and kidney growth in autosomal dominant polycystic kidney disease. N Engl J Med 2010, 363:820-829.
7. Leuenroth S.J., Okuhara D., Shotwell J.D., Markowitz G.S., Yu Z., Somlo S., et al. Triptolide is a traditional Chinese medicine-derived inhibitor of polycystic kidney disease. Proc Natl Acad Sci U S A 2007, 104:4389-4394.
8. Leuenroth S.J., Bencivenga N., Igarashi P., Somlo S., Crews C.M. Triptolide reduces cystogenesis in a model of ADPKD. J Am Soc Nephrol 2008, 19:1659-1662.
9. Mujumdar N., Saluja A.K. Autophagy in pancreatic cancer: an emerging mechanism of cell death. Autophagy 2010, 6:997-998.
10. Leonhard W.N., van der W.A., Novalic Z., Kunnen S.J., Gansevoort R.T., Breuning M.H., et al. Curcumin inhibits cystogenesis by simultaneous interference of multiple signaling pathways: in vivo evidence from a Pkd1-deletion model. Am J Physiol Renal Physiol 2011, 300:F1193-F1202.
11. Han J., Pan X.Y., Xu Y., Xiao Y., An Y., Tie L., et al. Curcumin induces autophagy to protect vascular endothelial cell survival from oxidative stress damage. Autophagy 2012, 8:812-825.
12. Cheng Y., Ren X., Zhang Y., Shan Y., Huber-Keener K.J., Zhang L., et al. Integrated regulation of autophagy and apoptosis by EEF2K controls cellular fate and modulates the efficacy of curcumin and velcade against tumor cells. Autophagy 2013, 9:208-219.
13. Talbot J.J., Shillingford J.M., Vasanth S., Doerr N., Mukherjee S., Kinter M.T., et al. Polycystin-1 regulates STAT activity by a dual mechanism. Proc Natl Acad Sci U S A. 2011, 108:7985-7990.
14. Pietrocola F., Izzo V., Niso-Santano M., Vacchelli E., Galluzi L., Maiuri M.C., et al. Regulation of autophagy by stress-responsive transcription factors. Semin Cancer Biol 2013, 23:310-322.
15. Bukanov N.O., Smith L.A., Klinger K.W., Ledbetter S.R., Ibraghimov-Beskrovnaya O. Long lasting arrest of murine polycystic kidney disease with CDK inhibitor rosocovitine. Nature 2006, 444:949-952.
16. Lambert L.A., Qiao N., Hunt K.K., Lambert D.H., Mills G.B., Meijer L., et al. Autophagy: a novel mechanism of synergistic cytotoxicity between doxorubicin and roscovitine in a sarcoma model. Cancer Res 2008, 68:7966-7974.
17. Chandrasekar B., Smith J.B., Freeman G.L. Ischemia-reperfusion of rat myocardium activates nuclear factor-kappaB and induces neutrophil infiltration via lipopolysaccharide-induced CXC chemokine. Circulation 2001, 103:2296-2302.
18. Sweeney W.E., von Vigier R.O., Frost P., Avner E.D. Src inhibition ameliorates polycystic kidney disease. J Am Soc Nephrol 2008, 19:1331-1341.
19. Fung C., Chen X., Grandis J.R., Duvvuri U. EGFR tyrosine kinase inhibition induces autophagy in cancer cells. Cancer Biol Ther 2012, 13:1417-1424.
20. Takiar V., Nishio S., Seo-Mayer P., King J.D., Li H., Zhang L., et al. Activating AMP-activated protein kinase (AMPK) slows renal cystogenesis. Proc Natl Acad Sci U S A 2011, 108:2462-2467.
21. Hoyer-Hansen M., Jaattela M. AMP-activated protein kinase: a universal regulator of autophagy?. Autophagy 2007, 3:381-383.
22. Xie Z., Lau K., Eby B., Lozano P., He C., Pennington B., et al. Improvement of cardiac functions by chronic metformin treatment is associated with enhanced cardiac autophagy in diabetic OVE26 mice. Diabetes 2011, 60:1770-1778.
23. Dai D.F., Rabinovitch P. Mitochondrial oxidative stress mediates induction of autophagy and hypertrophy in angiotensin-II treated mouse hearts. Autophagy 2011, 7:917-918.
24. Xiao R., Teng M., Zhang Q., Shi X.H., Huang Y.S. Myocardial autophagy after severe burn in rats. PLoS One 2012, 7:e39488.
25. Torres V.E., Chapman A.B., Devuyst O., Gansevoort R.T., Grantham J.J., Higashihara E., et al. Tolvaptan in patients with autosomal dominant polycystic kidney disease. N Engl J Med 2012, 367:2407-2418.
26. Wilson P.D. Polycystic kidney disease. N Engl J Med 2004, 350:151-164.
27. Edelstein C.L. What is the role of tubular epithelial cell apoptosis in polycystic kidney disease (PKD)?. Cell Cycle 2005, 4:e141-e145.
28. Narita M., Young A.R., Narita M. Autophagy facilitates oncogene-induced senescence. Autophagy 2009, 5:1046-1047.
29. Park J.Y., Park S.H., Weiss R.H. Disparate effects of roscovitine on renal tubular epithelial cell apoptosis and senescence: implications for autosomal dominant polycystic kidney disease. Am J Nephrol 2009, 29:509-515.
30. Yim N.H., Jung Y.P., Kim A., Ma C.J., Cho W.K., Ma JY Oyaksungisan, a traditional herbal formula, inhibits cell proliferation by induction of autophagy via JNK activation in human colon cancer cells. Evid Based Complement Alternat Med 2013, 2013:231874.
31. Giansanti V., Torriglia A., Scovassi A.I. Conversation between apoptosis and autophagy: "is it your turn or mine?". Apoptosis 2011, 16:321-333.
32. Kaushal G.P., Kaushal V., Herzog C., Yang C. Autophagy delays apoptosis in renal tubular epithelial cells in cisplatin cytotoxicity. Autophagy 2008, 4:710-712.
33. Boletta A., Qian F., Onuchic L.F., Bhunia A.K., Phakdeekitcharoen B., Hanaoka K., et al. Polycystin-1, the gene product of PKD1, induces resistance to apoptosis and spontaneous tubulogenesis in MDCK cells. Mol Cell 2000, 6:1267-1273.
34. Rowe I., Chiaravalli M., Mannella V., Ulisse V., Quilici G., Pema M., et al. Defective glucose metabolism in polycystic kidney disease identifies a new therapeutic strategy. Nat Med 2013, 19:488-493.
35. Belibi F., Ravichandran K., Bauer Segvic A., Jani A., Ljubanovic D., Edelstein C.L. Hypoxia-inducible factor 1 alpha and autophagy in polycystic kidney disease. Am J Physiol Renal Physiol 2011, 300:F1235-F1243.
36. Brown J.H., Bihoreau M.T., Hoffmann S., Kranzlin B., Tychinskaya I., Obermuller N., et al. Missense mutation in sterile alpha motif of novel protein SamCystin is associated with polycystic kidney disease in (cy/+) rat. J Am Soc Nephrol 2005, 9:937-945.
37. Neudecker S., Walz R., Menon K., Maier E., Bihoreau M.T., Obermuller N., et al. Transgenic overexpression of Anks6(p.R823W) causes polycystic kidney disease in rats. Am J Pathol 2010, 177:3000-3009.
38. Cao Y., Klionsky D.J. Physiological functions of Atg6/Beclin 1: a unique autophagy-related protein. Cell Res 2007, 17:839-849.
39. Bjorkoy G., Lamark T., Brech A., Outzen H., Perander M., Overvatn A., et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005, 171:603-614.
40. Woo D. Apoptosis and loss of renal tissue in polycystic kidney diseases. N Engl J Med 1995, 333:18-25.
41. Tao Y., Kim J., Faubel S., Wu J.C., Falk S.A., Schrier R.W., et al. Caspase inhibition reduces tubular apoptosis and proliferation and slows disease progression in polycystic kidney disease (PKD). Proc Natl Acad Sci U S A 2005, 102:6954-6959.
42. Tao Y., Zafar I., Kim J., Schrier R.W., Edelstein C.L. Deletion of the caspase-3 gene markedly prolongs survival in the cpk mouse model of polycystic kidney disease (PKD). J Am Soc Nephrol 2007, 19:749-755.
43. Mai W., Chen D., Ding T., Kim I., Park S., Cho S.Y., et al. Inhibition of Pkhd1 impairs tubulomorphogenesis of cultured IMCD cells. Mol Biol Cell 2005, 16:4398-4409.
44. Veis D.J., Sorenson C.M., Shutter J.R., Korsmeyer S.J. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 1993, 75:229-240.
45. Germain M., Slack R.S. Dining in with BCL-2: new guests at the autophagy table. Clin Sci 2010, 118:173-181.
46. Maiuri M.C., Le T.G., Criollo A., Rain J.C., Gautier F., Juin P., et al. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 2007, 26:2527-2539.
47. Saeki K., Yuo A., Okuma E., Yazaki Y., Susin S.A., Kroemer G., et al. Bcl-2 down-regulation causes autophagy in a caspase-independent manner in human leukemic HL60 cells. Cell Death Differ 2000, 7:1263-1269.
48. Shillingford J.M., Murcia N.S., Larson C.H., Low S.H., Hedgepeth R., Brown N., et al. The mTOR pathway is regulated by polycystin-1, and its inhibition reverses renal cystogenesis in polycystic kidney disease. Proc Natl Acad Sci U S A 2006, 103:5466-5471.
49. Natoli T.A., Smith L.A., Rogers K.A., Wang B., Komarnitsky S., Budman Y., et al. Inhibition of glucosylceramide accumulation results in effective blockade of polycystic kidney disease in mouse models. Nat Med 2010, 16:788-792.
50. Thoreen C.C., Sabatini D.M. Rapamycin inhibits mTORC1, but not completely. Autophagy 2009, 5:725-726.
51. Thoreen C.C., Kang S.A., Chang J.W., Liu Q., Zhang J., Gao Y., et al. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem 2009, 284:8023-8032.
52. Zhou F., Yang Y., Xing D. Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J 2011, 278:403-413.
53. Yu L., Alva A., Su H., Dutt P., Freundt E., Welsh S., et al. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 2004, 304:1500-1502.
54. Kroemer G., Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol 2008, 9:1004-1010.
55. Maiuri M.C., Zalckvar E., Kimchi A., Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007, 8:741-752.
56. Hotchkiss R.S., Strasser A., McDunn J.E., Swanson P.E. cell death. N Engl J Med 2009, 361:1570-1583.
57. Kotsis F., Boehlke C., Kuehn E.W. The ciliary flow sensor and polycystic kidney disease. Nephrol Dial Transplant 2013, 28:518-526.
58. Ko J.Y., Park J.H. Mouse models of polycystic kidney disease induced by defects of ciliary proteins. BMB Rep 2013, 46:73-79.
59. Winyard P., Jenkins D. Putative roles of cilia in polycystic kidney disease. Biochim Biophys Acta 2011, 1812:1256-1262.
60. Ma M., Tian X., Igarashi P., Pazour G.J., Somlo S. Loss of cilia suppresses cyst growth in genetic models of autosomal dominant polycystic kidney disease. Nat Genet 2013, 45:1004-1012.
61. Follit J.A., Tuft R.A., Fogarty K.E., Pazour G.J. The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol Biol Cell 2006, 17:3781-3792.
62. Jonassen J.A., SanAgustin J., Baker S.P., Pazour G.J. Disruption of IFT complex A causes cystic kidneys without mitotic spindle misorientation. J Am Soc Nephrol 2012, 23:641-651.
63. Jonassen J.A., San A.J., Follit J.A., Pazour G.J. Deletion of IFT20 in the mouse kidney causes misorientation of the mitotic spindle and cystic kidney disease. J Cell Biol 2008, 183:377-384.
64. Lin F., Hiesberger T., Cordes K., Sinclair A.M., Goldstein L.S., Somlo S., et al. Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proc Natl Acad Sci U S A 2003, 100:5286-5291.
65. Boehlke C., Kotsis F., Patel V., Braeg S., Voelker H., Bredt S., et al. Primary cilia regulate mTORC1 activity and cell size through Lkb1. Nat Cell Biol 2010, 12:1115-1122.
66. Zullo A., Iaconis D., Barra A., Cantone A., Messaddeq N., Capasso G., et al. Kidney-specific inactivation of Ofd1 leads to renal cystic disease associated with upregulation of the mTOR pathway. Hum Mol Genet 2010, 19:2792-2803.
67. Pampliega O., Orhon I., Patel B., Sridhar S., Diaz-Carretero A., Beau I., et al. Functional interaction between autophagy and ciliogenesis. Nature 2013, 502:194-200.
68. Tang Z., Lin M.G., Stowe T.R., Chen S., Zhu M., Stearns T., et al. Autophagy promotes primary ciliogenesis by removing OFD1 from centriolar satellites. Nature 2013, 502:254-257.