Urothelial defects from targeted inactivation of exocyst Sec10 in mice cause ureteropelvic junction obstructions

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Fogelgren, Ben ^a   Polgar, Noemi ^a   Lui, Vanessa H ^a   Lee, Amanda J ^a   Tamashiro, Kadee Kalia A ^a   Napoli, Josephine Andrea ^a   Walton, Chad B ^a   Zuo, Xiaofeng ^b   Lipschutz, Joshua H ^b,c  

^a UNIVERSITY OF HAWAII   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXOCYST; PROTEIN SEC10; UNCLASSIFIED DRUG; UROPLAKIN 3; EXOC5 PROTEIN, MOUSE; VESICULAR TRANSPORT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANURIA; ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE INACTIVATION; HYDRONEPHROSIS; MESENCHYME CELL; MORTALITY; MOUSE; NEWBORN; NONHUMAN; SEC10 GENE; URETER; URETEROPELVIC JUNCTION OBSTRUCTION; UROTHELIUM; ANIMAL; DISEASE MODEL; EMBRYOLOGY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; KIDNEY PELVIS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME FACTOR; TRANSGENIC MOUSE; URETER OBSTRUCTION; WESTERN BLOTTING;

MUS;

ANIMALS; ANIMALS, NEWBORN; ANURIA; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; HYDRONEPHROSIS; KIDNEY PELVIS; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS; URETERAL OBSTRUCTION; UROTHELIUM; VESICULAR TRANSPORT PROTEINS;

EID: 84935017962     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129346     Document Type: Article

References (73)

1. Benfield MR, McDonald RA, Bartosh S, Ho PL, Harmon W (2003) Changing trends in pediatric transplantation: 2001 Annual Report of the North American Pediatric Renal Transplant Cooperative Study. Pediatr Transplant 7: 321-335. PMID: 12890012
2. Woolf AS, Thiruchelvam N (2001) Congenital obstructive uropathy: its origin and contribution to endstage renal disease in children. Adv Ren Replace Ther 8: 157-163. PMID: 11533916
3. Collins AJ, Foley R, Herzog C, Chavers B, Gilbertson D, Ishani A, et al. (2008) Excerpts from the United States Renal Data System 2007 annual data report. Am J Kidney Dis 51: S1-320. doi: 10.1053/j.ajkd.2008.01.015 PMID: 18359402
4. Roth JA, Diamond DA (2001) Prenatal hydronephrosis. Curr Opin Pediatr 13: 138-141. PMID: 11317055
5. Woodward M, Frank D (2002) Postnatal management of antenatal hydronephrosis. BJU Int 89: 149-156. PMID: 11849184
6. Mesrobian HG, Mirza SP (2012) Hydronephrosis: a view from the inside. Pediatr Clin North Am 59: 839-851. doi: 10.1016/j.pcl.2012.05.008 PMID: 22857832
7. Roth KS, Koo HP, Spottswood SE, Chan JC (2002) Obstructive uropathy: an important cause of chronic renal failure in children. Clin Pediatr (Phila) 41: 309-314. PMID: 12086196
8. Klein J, Gonzalez J, Miravete M, Caubet C, Chaaya R, Decramer S, et al. (2011) Congenital ureteropelvic junction obstruction: human disease and animal models. Int J Exp Pathol 92: 168-192. doi: 10.1111/j.1365-2613.2010.00727.x PMID: 20681980
9. Ingraham SE, McHugh KM (2011) Current perspectives on congenital obstructive nephropathy. Pediatr Nephrol 26: 1453-1461. doi: 10.1007/s00467-011-1799-8 PMID: 21327776
10. Chevalier RL, Thornhill BA, Forbes MS, Kiley SC (2010) Mechanisms of renal injury and progression of renal disease in congenital obstructive nephropathy. Pediatr Nephrol 25: 687-697. doi: 10.1007/s00467-009-1316-5 PMID: 19844747
11. Dressler GR (2009) Advances in early kidney specification, development and patterning. Development 136: 3863-3874. doi: 10.1242/dev.034876 PMID: 19906853
12. Gandhi D, Molotkov A, Batourina E, Schneider K, Dan H, Reiley M, et al. (2013) Retinoid signaling in progenitors controls specification and regeneration of the urothelium. Dev Cell 26: 469-482. doi: 10.1016/j.devcel.2013.07.017 PMID: 23993789
13. Yamany T, Van Batavia J, Mendelsohn C (2014) Formation and regeneration of the urothelium. Curr Opin Organ Transplant 19: 323-330. doi: 10.1097/MOT.0000000000000084 PMID: 24752063
14. Airik R, Kispert A (2007) Down the tube of obstructive nephropathies: the importance of tissue interactions during ureter development. Kidney Int 72: 1459-1467. PMID: 17928823
15. Woolf AS, Davies JA (2013) Cell biology of ureter development. J Am Soc Nephrol 24: 19-25. doi: 10.1681/ASN.2012020127 PMID: 23123402
16. Khandelwal P, Abraham SN, Apodaca G (2009) Cell biology and physiology of the uroepithelium. Am J Physiol Renal Physiol 297: F1477-1501. doi: 10.1152/ajprenal.00327.2009 PMID: 19587142
17. Hu CC, Liang FX, Zhou G, Tu L, Tang CH, Zhou J, et al. (2005) Assembly of urothelial plaques: tetraspanin function in membrane protein trafficking. Mol Biol Cell 16: 3937-3950. PMID: 15958488
18. Mathai JC, Zhou EH, Yu W, Kim JH, Zhou G, Liao Y, et al. (2014) Hypercompliant apical membranes of bladder umbrella cells. Biophys J 107: 1273-1279. doi: 10.1016/j.bpj.2014.07.047 PMID: 25229135
19. Heider MR, Munson M (2012) Exorcising the Exocyst Complex. Traffic.
20. Lipschutz JH, Mostov KE (2002) Exocytosis: the many masters of the exocyst. Curr Biol 12: R212-214. PMID: 11909549
21. Wu H, Rossi G, Brennwald P (2008) The ghost in the machine: small GTPases as spatial regulators of exocytosis. Trends Cell Biol 18: 397-404. doi: 10.1016/j.tcb.2008.06.007 PMID: 18706813
22. Lyons PD, Peck GR, Kettenbach AN, Gerber SA, Roudaia L, Lienhard GE (2009) Insulin stimulates the phosphorylation of the exocyst protein Sec8 in adipocytes. Biosci Rep 29: 229-235. doi: 10.1042/BSR20080162 PMID: 19006485
23. Chen XW, Leto D, Xiao J, Goss J, Wang Q, Shavit JA, et al. (2011) Exocyst function is regulated by effector phosphorylation. Nat Cell Biol 13: 580-588. doi: 10.1038/ncb2226 PMID: 21516108
24. Ren J, Guo W (2012) ERK1/2 regulate exocytosis through direct phosphorylation of the exocyst component Exo70. Dev Cell 22: 967-978. doi: 10.1016/j.devcel.2012.03.005 PMID: 22595671
25. Guo W, Roth D, Walch-Solimena C, Novick P (1999) The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J 18: 1071-1080. PMID: 10022848
26. Lipschutz JH, Guo W, O'Brien LE, Nguyen YH, Novick P, Mostov KE (2000) Exocyst Is involved in cystogenesis and tubulogenesis and acts by modulating synthesis and delivery of basolateral plasma membrane and secretory proteins. Mol Biol Cell 11: 4259-4275. PMID: 11102522
27. Zuo X, Guo W, Lipschutz JH (2009) The Exocyst Protein Sec10 Is Necessary for Primary Ciliogenesis and Cystogenesis In Vitro. Mol Biol Cell 20: 2522-2529. doi: 10.1091/mbc.E08-07-0772 PMID: 19297529
28. Fogelgren B, Lin SY, Zuo X, Jaffe KM, Park KM, Reichert RJ, et al. (2011) The exocyst protein Sec10 interacts with Polycystin-2 and knockdown causes PKD-phenotypes. PLoS Genet 7: e1001361. doi: 10.1371/journal.pgen.1001361 PMID: 21490950
29. Zuo X, Fogelgren B, Lipschutz JH (2011) The small GTPase Cdc42 is necessary for primary ciliogenesis in renal tubular epithelial cells. J Biol Chem 286: 22469-22477. doi: 10.1074/jbc.M111.238469 PMID: 21543338
30. Park KM, Fogelgren B, Zuo X, Kim J, Chung DC, Lipschutz JH (2010) Exocyst Sec10 protects epithelial barrier integrity and enhances recovery following oxidative stress, by activation of the MAPK pathway. Am J Physiol Renal Physiol 298: F818-826. doi: 10.1152/ajprenal.00596.2009 PMID: 20053792
31. Friedrich GA, Hildebrand JD, Soriano P (1997) The secretory protein Sec8 is required for paraxial mesoderm formation in the mouse. Dev Biol 192: 364-374. PMID: 9441674
32. Friedel RH, Seisenberger C, Kaloff C, Wurst W (2007) EUCOMM-the European conditional mouse mutagenesis program. Brief Funct Genomic Proteomic 6: 180-185. PMID: 17967808
33. Farley FW, Soriano P, Steffen LS, Dymecki SM (2000) Widespread recombinase expression using FLPeR (flipper) mice. Genesis 28: 106-110. PMID: 11105051
34. Schwenk F, Baron U, Rajewsky K (1995) A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23: 5080-5081. PMID: 8559668
35. Shao X, Somlo S, Igarashi P (2002) Epithelial-specific Cre-lox recombination in the developing kidney and genitourinary tract. J Am Soc Nephrol 13: 1837-1846. PMID: 12089379
36. Shao X, Johnson JE, Richardson JA, Hiesberger T, Igarashi P (2002) A minimal Ksp-cadherin promoter linked to a green fluorescent protein reporter gene exhibits tissue-specific expression in the developing kidney and genitourinary tract. J Am Soc Nephrol 13: 1824-1836. PMID: 12089378
37. Igarashi P (2003) Following the expression of a kidney-specific gene from early development to adulthood. Nephron Exp Nephrol 94: e1-6. PMID: 12806181
38. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, et al. (2010) A robust and highthroughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133-140. doi: 10.1038/nn.2467 PMID: 20023653
39. Li L, Zepeda-Orozco D, Patel V, Truong P, Karner CM, Carroll TJ, et al. (2009) Aberrant planar cell polarity induced by urinary tract obstruction. Am J Physiol Renal Physiol 297: F1526-1533. doi: 10.1152/ajprenal.00318.2009 PMID: 19794107
40. Bascands JL, Schanstra JP (2005) Obstructive nephropathy: insights from genetically engineered animals. Kidney Int 68: 925-937. PMID: 16105023
41. Novick P, Ferro S, Schekman R (1981) Order of events in the yeast secretory pathway. Cell 25: 461-469. PMID: 7026045
42. Novick P, Field C, Schekman R (1980) Identification of 23 complementation groups required for posttranslational events in the yeast secretory pathway. Cell 21: 205-221. PMID: 6996832
43. Novick P, Schekman R (1979) Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 76: 1858-1862. PMID: 377286
44. Inoue M, Chang L, Hwang J, Chiang S, Saltiel AR (2003) The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature 422: 629-633. PMID: 12687004
45. Vega IE, Hsu SC (2001) The exocyst complex associates with microtubules to mediate vesicle targeting and neurite outgrowth. J Neurosci 21: 3839-3848. PMID: 11356872
46. Letinic K, Sebastian R, Toomre D, Rakic P (2009) Exocyst is involved in polarized cell migration and cerebral cortical development. Proc Natl Acad Sci U S A 106: 11342-11347. doi: 10.1073/pnas.0904244106 PMID: 19549839
47. Nichols CD, Casanova JE (2010) Salmonella-directed recruitment of new membrane to invasion foci via the host exocyst complex. Curr Biol 20: 1316-1320. doi: 10.1016/j.cub.2010.05.065 PMID: 20579884
48. Guichard A, Cruz-Moreno B, Aguilar B, van Sorge NM, Kuang J, Kurkciyan AA, et al. (2013) Cholera toxin disrupts barrier function by inhibiting exocyst-mediated trafficking of host proteins to intestinal cell junctions. Cell Host Microbe 14: 294-305. doi: 10.1016/j.chom.2013.08.001 PMID: 24034615
49. Guichard A, McGillivray SM, Cruz-Moreno B, van Sorge NM, Nizet V, Bier E (2010) Anthrax toxins cooperatively inhibit endocytic recycling by the Rab11/Sec15 exocyst. Nature 467: 854-858. doi: 10.1038/nature09446 PMID: 20944747
50. Lu H, Liu J, Liu S, Zeng J, Ding D, Carstens RP, et al. (2013) Exo70 isoform switching upon epithelial-mesenchymal transition mediates cancer cell invasion. Dev Cell 27: 560-573. doi: 10.1016/j.devcel.2013.10.020 PMID: 24331928
51. Thapa N, Sun Y, Schramp M, Choi S, Ling K, Anderson RA (2012) Phosphoinositide signaling regulates the exocyst complex and polarized integrin trafficking in directionally migrating cells. Dev Cell 22: 116-130. doi: 10.1016/j.devcel.2011.10.030 PMID: 22264730
52. Liu J, Yue P, Artym VV, Mueller SC, Guo W (2009) The role of the exocyst in matrix metalloproteinase secretion and actin dynamics during tumor cell invadopodia formation. Mol Biol Cell 20: 3763-3771. doi: 10.1091/mbc.E08-09-0967 PMID: 19535457
53. Bodemann BO, Orvedahl A, Cheng T, Ram RR, Ou YH, Formstecher E, et al. (2011) RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly. Cell 144: 253-267. doi: 10.1016/j.cell.2010.12.018 PMID: 21241894
54. Roth D, Guo W, Novick P (1998) Dominant negative alleles of SEC10 reveal distinct domains involved in secretion and morphogenesis in yeast. Mol Biol Cell 9: 1725-1739. PMID: 9658167
55. Erman A, Veranic P, Psenicnik M, Jezernik K (2006) Superficial cell differentiation during embryonic and postnatal development of mouse urothelium. Tissue Cell 38: 293-301. PMID: 16973199
56. Khandelwal P, Prakasam HS, Clayton DR, Ruiz WG, Gallo LI, van Roekel D, et al. (2013) A Rab11a-Rab8a-Myo5B network promotes stretch-regulated exocytosis in bladder umbrella cells. Mol Biol Cell 24: 1007-1019. doi: 10.1091/mbc.E12-08-0568 PMID: 23389633
57. Khandelwal P, Ruiz WG, Balestreire-Hawryluk E, Weisz OA, Goldenring JR, Apodaca G (2008) Rab11a-dependent exocytosis of discoidal/fusiform vesicles in bladder umbrella cells. Proc Natl Acad Sci U S A 105: 15773-15778. doi: 10.1073/pnas.0805636105 PMID: 18843107
58. Bartoli FA, Paradies G, Leggio A, Virgintino D, Bertossi M, Roncali L (1996) Urothelium damage as the primary cause of ureteropelvic junction obstruction: a new hypothesis. Urol Res 24: 9-13. PMID: 8966845
59. Kong XT, Deng FM, Hu P, Liang FX, Zhou G, Auerbach AB, et al. (2004) Roles of uroplakins in plaque formation, umbrella cell enlargement, and urinary tract diseases. J Cell Biol 167: 1195-1204. PMID: 15611339
60. Hu P, Deng FM, Liang FX, Hu CM, Auerbach AB, Shapiro E, et al. (2000) Ablation of uroplakin III gene results in small urothelial plaques, urothelial leakage, and vesicoureteral reflux. J Cell Biol 151: 961-972. PMID: 11085999
61. Singh S, Robinson M, Nahi F, Coley B, Robinson ML, Bates CM, et al. (2007) Identification of a unique transgenic mouse line that develops megabladder, obstructive uropathy, and renal dysfunction. J Am Soc Nephrol 18: 461-471. PMID: 17202422
62. Ingraham SE, Saha M, Carpenter AR, Robinson M, Ismail I, Singh S, et al. (2010) Pathogenesis of renal injury in the megabladder mouse: a genetic model of congenital obstructive nephropathy. Pediatr Res 68: 500-507. doi: 10.1203/PDR.0b013e3181f82f15 PMID: 20736884
63. Chang CP, McDill BW, Neilson JR, Joist HE, Epstein JA, Crabtree GR, et al. (2004) Calcineurin is required in urinary tract mesenchyme for the development of the pyeloureteral peristaltic machinery. J Clin Invest 113: 1051-1058. PMID: 15057312
64. Aoki Y, Mori S, Kitajima K, Yokoyama O, Kanamaru H, Okada K, et al. (2004) Id2 haploinsufficiency in mice leads to congenital hydronephrosis resembling that in humans. Genes Cells 9: 1287-1296. PMID: 15569159
65. Tripathi P, Wang Y, Casey AM, Chen F (2012) Absence of canonical Smad signaling in ureteral and bladder mesenchyme causes ureteropelvic junction obstruction. J Am Soc Nephrol 23: 618-628. doi: 10.1681/ASN.2011060566 PMID: 22282597
66. Yu J, Carroll TJ, McMahon AP (2002) Sonic hedgehog regulates proliferation and differentiation of mesenchymal cells in the mouse metanephric kidney. Development 129: 5301-5312. PMID: 12399320
67. Cain JE, Islam E, Haxho F, Blake J, Rosenblum ND (2011) GLI3 repressor controls functional development of the mouse ureter. J Clin Invest 121: 1199-1206. doi: 10.1172/JCI45523 PMID: 21339645
68. Haraguchi R, Matsumaru D, Nakagata N, Miyagawa S, Suzuki K, Kitazawa S, et al. (2012) The hedgehog signal induced modulation of bone morphogenetic protein signaling: an essential signaling relay for urinary tract morphogenesis. PLoS One 7: e42245. doi: 10.1371/journal.pone.0042245 PMID: 22860096
69. Lloyd KC (2011) A knockout mouse resource for the biomedical research community. Ann N Y Acad Sci 1245: 24-26. doi: 10.1111/j.1749-6632.2011.06311.x PMID: 22211970
70. Whyte DA, Li C, Thomson RB, Nix SL, Zanjani R, Karp SL, et al. (1999) Ksp-cadherin gene promoter. I. Characterization and renal epithelial cell-specific activity. Am J Physiol 277: F587-598. PMID: 10516284
71. Igarashi P, Shashikant CS, Thomson RB, Whyte DA, Liu-Chen S, Ruddle FH, et al. (1999) Ksp-cadherin gene promoter. II. Kidney-specific activity in transgenic mice. Am J Physiol 277: F599-610. PMID: 10516285
72. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675. PMID: 22930834
73. Fogelgren B, Yang S, Sharp IC, Huckstep OJ, Ma W, Somponpun SJ, et al. (2009) Deficiency in Six2 during prenatal development is associated with reduced nephron number, chronic renal failure, and hypertension in Br/+ adult mice. Am J Physiol Renal Physiol 296: F1166-1178. doi: 10.1152/ajprenal. 90550.2008 PMID: 19193724