MicroRNAs in the pathogenesis of cystic kidney disease

Current Opinion in Pediatrics

Volumn 27, Issue 2, 2015, Pages 219-226

  Phua, Yu Leng ^a,b   Ho, Jacqueline ^a,b  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

cystic kidney disease; miRNA; polycystic kidney disease; post transcriptional regulation

Indexed keywords

MICRORNA; MICRORNA 17; MICRORNA 92A; UNCLASSIFIED DRUG; BIOLOGICAL MARKER;

AUTOSOMAL RECESSIVE DISORDER; BICC1 GENE; GENE; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; KIDNEY DEVELOPMENT; KIDNEY POLYCYSTIC DISEASE; LIN28 LET7 GENE; NEPHROBLASTOMA; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; VON HIPPEL LINDAU DISEASE; GENETICS; KIDNEY; KIDNEY TUMOR; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

BIOMARKERS; HUMANS; KIDNEY; KIDNEY NEOPLASMS; MICRORNAS; POLYCYSTIC KIDNEY DISEASES; VON HIPPEL-LINDAU DISEASE; WILMS TUMOR;

EID: 84916238670     PISSN: 10408703     EISSN: 1531698X     Source Type: Journal    
DOI: 10.1097/MOP.0000000000000168     Document Type: Review

References (78)

1. Masoumi A, Reed-Gitomer B, Kelleher C,. et al. Developments in the management of autosomal dominant polycystic kidney disease. Ther Clin Risk Manag 2008; 4: 393-407
2. Woo D. Apoptosis and loss of renal tissue in polycystic kidney diseases. N Engl J Med 1995; 333: 18-25
3. Fischer E, Legue E, Doyen A,. et al. Defective planar cell polarity in polycystic kidney disease. Nat Genet 2006; 38: 21-23
4. Avner ED, Sweeney WE Jr, Nelson WJ. Abnormal sodium pump distribution during renal tubulogenesis in congenital murine polycystic kidney disease. Proc Natl Acad Sci U S A 1992; 89: 7447-7451
5. Saburi S, Hester I, Fischer E,. et al. Loss of fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat Genet 2008; 40: 1010-1015
6. Hanaoka K, Guggino WB. Camp regulates cell proliferation and cyst formation in autosomal polycystic kidney disease cells. J Am Soc Nephrol 2000; 11: 1179-1187
7. Pazour GJ, Dickert BL, Vucica Y,. et al. Chlamydomonas Ift88 and its mouse homologue, polycystic kidney disease gene Tg737, are required for assembly of cilia and flagella. J Cell Biol 2000; 151: 709-718
8. Yoder BK, Hou X, Guay-Woodford LM. The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia. J Am Soc Nephrol 2002; 13: 2508-2516
9. Hou X, Mrug M, Yoder BK,. et al. Cystin, a novel cilia-associated protein, is disrupted in the Cpk mouse model of polycystic kidney disease. J Clin Invest 2002; 109: 533-540
10. Low SH, Vasanth S, Larson CH,. et al. Polycystin-1, Stat6, and P100 function in a pathway that transduces ciliary mechanosensation and is activated in polycystic kidney disease. Dev Cell 2006; 10: 57-69
11. Nauli SM, Alenghat FJ, Luo Y,. et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 2003; 33: 129-137
12. Koulen P, Cai Y, Geng L,. et al. Polycystin-2 is an intracellular calcium release channel. Nat Cell Biol 2002; 4: 191-197
13. Phua YL, Martel N, Pennisi DJ,. et al. Distinct sites of renal fibrosis in crim1 mutant mice arise from multiple cellular origins. J Pathol 2013; 229: 685-696
14. Okada H, Ban S, Nagao S,. et al. Progressive renal fibrosis in murine polycystic kidney disease: an immunohistochemical observation. Kidney Int 2000; 58: 587-597
15. Burn TC, Connors TD, Dackowski WR,. et al. Analysis of the genomic sequence for the autosomal dominant polycystic kidney disease (PKD1) gene predicts the presence of a leucine-rich repeat. The American Pkd1 Consortium (APKD1 Consortium). Hum Mol Genet 1995; 4: 575-582
16. Hughes J, Ward CJ, Peral B,. et al. The polycystic kidney disease 1 (PKD1) gene encodes a novel protein with multiple cell recognition domains. Nat Genet 1995; 10: 151-160
17. Mochizuki T, Wu GQ, Hayashi T,. et al. PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 1996; 272: 1339-1342
18. Brasier JL, Henske EP. Loss of the polycystic kidney disease (PKD1) region of chromosome 16p13 in renal cyst cells supports a loss-of-function model for cyst pathogenesis. J Clin Invest 1997; 99: 194-199
19. González-Perrett S, Kim K, Ibarra C,. et al. Polycystin-2, the protein mutated in autosomal dominant polycystic kidney disease (ADPKD), is a Ca2-permeable nonselective cation channel. Proc Natl Acad Sci U S A 2001; 98: 1182-1187
20. Boucher C, Sandford R. Autosomal dominant polycystic kidney disease (ADPKD, MIM 173900, PKD1 and PKD2 genes, protein products known as polycystin-1 and polycystin-2). Eur J Hum Genet 2004; 12: 347-354
21. Bergmann C, Senderek J, Küpper F,. et al. PKHD1 mutations in autosomal recessive polycystic kidney disease (ARPKD). Human Mutat 2004; 23: 453-463
22. Bellanne-Chantelot C, Chauveau D, Gautier JF,. et al. Clinical spectrum associated with hepatocyte nuclear factor-1beta mutations. Ann Intern Med 2004; 140: 510-517
23. Otto EA, Trapp ML, Schultheiss UT,. et al. Nek8 mutations affect ciliary and centrosomal localization and may cause nephronophthisis. J Am Soc Nephrol 2008; 19: 587-592
24. Nagalakshmi VK, Ren Q, Pugh MM,. et al. Dicer regulates the development of nephrogenic and ureteric compartments in the mammalian kidney. Kidney Int 2011; 79: 317-330
25. Patel V, Williams D, Hajarnis S,. et al. Mir-17-92 miRNA cluster promotes kidney cyst growth in polycystic kidney disease. Proc Natl Acad Sci U S A 2013; 110: 10765-10770
26. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-297
27. Lee Y, Ahn C, Han J,. et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003; 425: 415-419
28. Hutvagner G, McLachlan J, Pasquinelli AE,. et al. A cellular function for the RNA-interference enzyme dicer in the maturation of the Let-7 small temporal RNA. Science 2001; 293: 834-838
29. Ketting RF, Fischer SE, Bernstein E,. et al. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 2001; 15: 2654-2659
30. Ho J, Kreidberg JA. The long and short of microRNAs in the kidney. J Am Soc Nephrol 2012; 23: 400-404
31. Grimson A, Farh KK, Johnston WK,. et al. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 2007; 27: 91-105
32. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120: 15-20
33. Hammond SM, Bernstein E, Beach D,. et al. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 2000; 404: 293-296
34. Ho J, Pandey P, Schatton T,. et al. The pro-apoptotic protein Bim is a microRNA target in kidney progenitors. J Am Soc Nephrol 2011; 22: 1053-1063
35. Pastorelli LM, Wells S, Fray M,. et al. Genetic analyses reveal a requirement for Dicer1 in the mouse urogenital tract. Mamm Genome 2009; 20: 140-151
36. Shi S, Yu L, Chiu C,. et al. Podocyte-selective deletion of dicer induces proteinuria and glomerulosclerosis. J Am Soc Nephrol 2008; 19: 2159-2169
37. Harvey SJ, Jarad G, Cunningham J,. et al. Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol 2008; 19: 2150-2158
38. Ho J, Ng KH, Rosen S,. et al. Podocyte-specific loss of functional microRNAs leads to rapid glomerular and tubular injury. J Am Soc Nephrol 2008; 19: 2069-2075
39. Zhdanova O, Srivastava S, Di L,. et al. The inducible deletion of drosha and microRNAs in mature podocytes results in a collapsing glomerulopathy. Kidney Int 2011; 80: 719-730
40. Wei Q, Bhatt K, He HZ,. et al. Targeted deletion of dicer from proximal tubules protects against renal ischemia-reperfusion injury. J Am Soc Nephrol 2010; 21: 756-761
41. Sequeira-Lopez ML, Weatherford ET, Borges GR,. et al. The microRNAprocessing enzyme dicer maintains juxtaglomerular cells. J Am Soc Nephrol 2010; 21: 460-467
42. Tran U, Zakin L, Schweickert A,. et al. The RNA-binding protein bicaudal C regulates polycystin 2 in the kidney by antagonizing mir-17 activity. Development 2010; 137: 1107-1116
43. Piazzon N, Maisonneuve C, Guilleret I,. et al. Bicc1 links the regulation of camp signaling in polycystic kidneys to microRNA-induced gene silencing. J Mol Cell Biol 2012; 4: 398-408
44. Duan J, Huang H, Lv X,. et al. PKHD1 post-transcriptionally modulated by mir-365-1 inhibits cell-cell adhesion. Cell Biochem Funct 2012; 30: 382-389
45. Enright AJ, John B, Gaul U,. et al. MicroRNA targets in Drosophila. Genome Biol 2004; 5: R1-R11
46. Paraskevopoulou MD, Georgakilas G, Kostoulas N,. et al. DIANA-microT Web Server V5.0: service integration into miRNA functional analysis workflows. Nucleic Acids Res 2013; 41 (Web Server issue): W169-W173
47. Pandey P, Qin S, Ho J,. et al. Systems biology approach to identify transcriptome reprogramming and candidate microRNA targets during the progression of polycystic kidney disease. BMC Syst Biol 2011; 5: 56
48. Pandey P, Brors B, Srivastava PK,. et al. Microarray-based approach identifies microRNAs and their target functional patterns in polycystic kidney disease. BMC Genomics 2008; 9: 624
49. De Pontual L, Yao E, Callier P,. et al. Germline deletion of the mir-17-92 cluster causes skeletal and growth defects in humans. Nat Genet 2011; 43: 1026-1030
50. ODonnell KA, Wentzel EA, Zeller KI,. et al. c-Myc-regulated microRNAs modulate E2f1 expression. Nature 2005; 435: 839-843
51. Celli J, van Bokhoven H, Brunner HG. Feingold syndrome: clinical review and genetic mapping. Am J Med Genet A 2003; 122A: 294-300
52. Marcelis CL, Hol FA, Graham GE,. et al. Genotype-phenotype correlations in Mycn-related Feingold syndrome. Hum Mutat 2008; 29: 1125-1132
53. Gnarra JR, Tory K, Weng Y,. et al. Mutations of the VHL tumour suppressor gene in renal carcinoma. Nat Genet 1994; 7: 85-90
54. Lonser RR, Glenn GM, Walther M,. et al. Von Hippel-Lindau disease. Lancet 2003; 361: 2059-2067
55. Ghosh AK, Shanafelt TD, Cimmino A,. et al. Aberrant regulation of pVHL levels by microRNA promotes the HIF/VEGF axis in CLL B cells. Blood 2009; 113: 5568-5574
56. Marrone AK, Stolz DB, Bastacky SI,. et al. MicroRNA-17-92 is required for nephrogenesis and renal function. J Am Soc Nephrol 2014; 25: 1440-1452
57. Cloonan N, Brown MK, Steptoe AL,. et al. The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol 2008; 9: R127
58. Fontana L, Fiori ME, Albini S,. et al. Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and Bim. PLoS One 2008; 3: e2236
59. Wong P, Iwasaki M, Somervaille TC,. et al. The mir-17-92 microRNA polycistron regulates MLL leukemia stem cell potential by modulating p21 expression. Cancer Res 2010; 70: 3833-3842
60. Gibcus JH, Kroesen BJ, Koster R,. et al. MiR-17/106b seed family regulates p21 in Hodgkins lymphoma. J Pathol 2011; 225: 609-617
61. Lee SO, Masyuk T, Splinter P,. et al. Microrna15a modulates expression of the cell-cycle regulator Cdc25a and affects hepatic cystogenesis in a rat model of polycystic kidney disease. J Clin Invest 2008; 118: 3714-3724
62. Urbach A, Yermalovich A, Zhang J,. et al. Lin28 sustains early renal progenitors and induces Wilms tumor. Genes Dev 2014; 28: 971-982
63. Lin F, Hiesberger T, Cordes K,. 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
64. Maisonneuve C, Guilleret I, Vick P,. et al. Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow. Development 2009; 136: 3019-3030
65. Mahone M, Saffman EE, Lasko PF. Localized bicaudal-C RNA encodes a protein containing a KH domain, the RNA binding motif of FMR1. EMBO J 1995; 14: 2043-2055
66. Shan SW, Lee DY, Deng Z,. et al. MicroRNA miR-17 retards tissue growth and represses fibronectin expression. Nat Cell Biol 2009; 11: 1031-1038
67. Jinno S, Suto K, Nagata A,. et al. Cdc25a is a novel phosphatase functioning early in the cell-cycle. EMBO J 1994; 13: 1549-1556
68. Joshi VV, Beckwith JB. Multilocular cyst of the kidney (cystic nephroma) and cystic, partially differentiated nephroblastoma. Terminology and criteria for diagnosis. Cancer 1989; 64: 466-479
69. Viswanathan SR, Daley GQ, Gregory RI. Selective blockade of microRNA processing by Lin28. Science 2008; 320: 97-100
70. Newman MA, Thomson JM, Hammond SM. Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 2008; 14: 1539-1549
71. Wilbert ML, Huelga SC, Kapeli K,. et al. Lin28 binds messenger RNAs at Ggaga motifs and regulates splicing factor abundance. Molecular Cell 2012; 48: 195-206
72. Viswanathan SR, Powers JT, Einhorn W,. et al. Lin28 promotes transformation and is associated with advanced human malignancies. Nat Genet 2009; 41: 843-848
73. Rakheja D, Chen KS, Liu Y,. et al. Somatic mutations in DROSHA and DICER1 impair microRNA biogenesis through distinct mechanisms in Wilms tumours. Nat Comm 2014; 2: .
74. Piskounova E, Viswanathan SR, Janas M,. et al. Determinants of microRNA processing inhibition by the developmentally regulated RNA-binding protein Lin28. J Biol Chem 2008; 283: 21310-21314
75. Cheng L, Sun X, Scicluna BJ,. et al. Characterization and deep sequencing analysis of exosomal and non-exosomal miRNA in human urine. Kidney Int 2014; 86: 433-444
76. Song X, Di Giovanni V, He N,. et al. Systems biology of autosomal dominant polycystic kidney disease (ADPKD): computational identification of gene expression pathways and integrated regulatory networks. Hum Mol Genet 2009; 18: 2328-2343
77. Ben-Dov IZ, Tan YC, Morozov P,. et al. Urine MicroRNA as potential biomarkers of autosomal dominant polycystic kidney disease progression: description of miRNA profiles at baseline. PLoS One 2014; 9: e86856
78. Chau BN, Xin C, Hartner J,. et al. MicroRNA-21 promotes fibrosis of the kidney by silencing metabolic pathways. Sci Transl Med 2012; 4: 121ra118