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Tuberous sclerosis complex exhibits a new renal cystogenic mechanism
dc.contributor.authorBissler, John J.
dc.contributor.authorZadjali, Fahad
dc.contributor.authorBridges, Dave
dc.contributor.authorAstrinidis, Aristotelis
dc.contributor.authorBarone, Sharon
dc.contributor.authorYao, Ying
dc.contributor.authorRedd, JeAnna R.
dc.contributor.authorSiroky, Brian J.
dc.contributor.authorWang, Yanqing
dc.contributor.authorFinley, Joel T.
dc.contributor.authorRusiniak, Michael E.
dc.contributor.authorBaumann, Heinz
dc.contributor.authorZahedi, Kamyar
dc.contributor.authorGross, Kenneth W.
dc.contributor.authorSoleimani, Manoocher
dc.date.accessioned2019-02-12T20:23:33Z
dc.date.available2020-03-03T21:29:36Zen
dc.date.issued2019-01
dc.identifier.citationBissler, John J.; Zadjali, Fahad; Bridges, Dave; Astrinidis, Aristotelis; Barone, Sharon; Yao, Ying; Redd, JeAnna R.; Siroky, Brian J.; Wang, Yanqing; Finley, Joel T.; Rusiniak, Michael E.; Baumann, Heinz; Zahedi, Kamyar; Gross, Kenneth W.; Soleimani, Manoocher (2019). "Tuberous sclerosis complex exhibits a new renal cystogenic mechanism." Physiological Reports (2): n/a-n/a.
dc.identifier.issn2051-817X
dc.identifier.issn2051-817X
dc.identifier.urihttps://hdl.handle.net/2027.42/147796
dc.description.abstractTuberous sclerosis complex (TSC) is a tumor predisposition syndrome with significant renal cystic and solid tumor disease. While the most common renal tumor in TSC, the angiomyolipoma, exhibits a loss of heterozygosity associated with disease, we have discovered that the renal cystic epithelium is composed of type A intercalated cells that have an intact Tsc gene that have been induced to exhibit Tsc‐mutant disease phenotype. This mechanism appears to be different than that for ADPKD. The murine models described here closely resemble the human disease and both appear to be mTORC1 inhibitor responsive. The induction signaling driving cystogenesis may be mediated by extracellular vesicle trafficking.TSC renal cystic disease develops in about half of the patients. The disease appears to caused by an induction mechanism such that a small population of mutant cells can cause significant renal cystic disease comprised of mostly genetically normal cells.
dc.publisherWiley Periodicals, Inc.
dc.publisherSpringer
dc.subject.otherrenal cystogenesis
dc.subject.otherrenal cystic disease
dc.subject.otherIntercalated cells
dc.subject.otherTuberous sclerosis complex
dc.titleTuberous sclerosis complex exhibits a new renal cystogenic mechanism
dc.typeArticleen_US
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelPhysiology
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/147796/1/phy213983.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/147796/2/phy213983_am.pdf
dc.identifier.doi10.14814/phy2.13983
dc.identifier.sourcePhysiological Reports
dc.identifier.citedreferenceRakowski, S. K., E. B. Winterkorn, E. Paul, D. J. Steele, E. F. Halpern, and E. A. Thiele. 2006. Renal manifestations of tuberous sclerosis complex: incidence, prognosis, and predictive factors. Kidney Int. 70: 1777 – 1782.
dc.identifier.citedreferenceQuesenberry, P. J., J. Aliotta, M. C. Deregibus, and G. Camussi. 2015. Role of extracellular RNA‐carrying vesicles in cell differentiation and reprogramming. Stem Cell Res. Ther. 6: 153.
dc.identifier.citedreferenceRajagopal, M., S. V. Thomas, P. P. Kathpalia, Y. Chen, and A. C. Pao. 2014. Prostaglandin E2 induces chloride secretion through crosstalk between cAMP and calcium signaling in mouse inner medullary collecting duct cells. Am. J. Physiol. Cell Physiol. 306: C263 – C278.
dc.identifier.citedreferenceRamkumar, N., and D. E. Kohan. 2016a. The nephron (pro)renin receptor: function and significance. Am. J. Physiol. Renal Physiol. 311: F1145 – F1148.
dc.identifier.citedreferenceRamkumar, N., and D. E. Kohan. 2016b. Role of the collecting duct renin angiotensin system in regulation of blood pressure and renal function. Curr. Hypertens. Rep. 18: 29.
dc.identifier.citedreferencevan Rooijen, E., G. van de Hoek, I. Logister, H. Ajzenberg, N. Knoers, F. van Eeden, et al. 2018. The von hippel‐lindau gene is required to maintain renal proximal tubule and glomerulus integrity in zebrafish larvae. Nephron 138: 310 – 323.
dc.identifier.citedreferenceRoux, T., I. An‐Gourfinkel, A. Bertrand, and F. Bielle. 2017. Astrocytic tumor with large cells and worrisome features in two patients with tuberous sclerosis: drastically different diagnoses and prognoses. Clin. Neuropathol. 36 ( 2017 ): 102 – 107.
dc.identifier.citedreferenceRoy, A., M. M. Al‐bataineh, and N. M. Pastor‐Soler. 2015. Collecting duct intercalated cell function and regulation. Clin. J. Am. Soc. Nephrol. 10: 305 – 324.
dc.identifier.citedreferenceSaigusa, T., Y. Dang, M. A. Bunni, M. Y. Amria, S. L. Steele, W. R. Fitzgibbon, et al. 2015. Activation of the intrarenal renin‐angiotensin‐system in murine polycystic kidney disease. Physiol. Rep. 3: e12405.
dc.identifier.citedreferenceSancak, Y., L. Bar‐Peled, R. Zoncu, A. L. Markhard, S. Nada, and D. M. Sabatini. 2010. Ragulator‐Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141: 290 – 303.
dc.identifier.citedreferenceScheffers, M. S., P. van der Bent, F. Prins, L. Spruit, M. H. Breuning, S. V. Litvinov, et al. 2000. Polycystin‐1, the product of the polycystic kidney disease 1 gene, co‐localizes with desmosomes in MDCK cells. Hum. Mol. Genet. 9: 2743 – 2750.
dc.identifier.citedreferenceSeva Pessoa, B., N. van der Lubbe, K. Verdonk, A. J. Roks, E. J. Hoorn, and A. H. Danser. 2013. Key developments in renin‐angiotensin‐aldosterone system inhibition. Nat. Rev. Nephrol. 9: 26 – 36.
dc.identifier.citedreferenceSihn, G., C. Burckle, A. Rousselle, T. Reimer, and M. Bader. 2013. (Pro)renin receptor: subcellular localizations and functions. Front. Biosci. (Elite Ed) 5: 500 – 508.
dc.identifier.citedreferenceSiroky, B. J., M. F. Czyzyk‐Krzeska, and J. J. Bissler. 2009. Renal involvement in tuberous sclerosis complex and von hippel‐lindau disease: shared disease mechanisms? Nat. Clin. Pract. Nephrol. 5: 143 – 156.
dc.identifier.citedreferenceSiroky, B. J., H. Yin, J. T. Babcock, L. Lu, A. R. Hellmann, B. P. Dixon, et al. 2012. Human TSC‐associated renal angiomyolipoma cells are hypersensitive to ER stress. Am. J. Physiol. Renal Physiol. 303: F831 – F844.
dc.identifier.citedreferenceSiroky, B. J., H. Yin, B. P. Dixon, R. J. Reichert, A. R. Hellmann, T. Ramkumar, et al. 2014. Evidence for pericyte origin of TSC‐associated renal angiomyolipomas and implications for angiotensin receptor inhibition therapy. Am. J. Physiol. Renal Physiol. 307: F560 – F570.
dc.identifier.citedreferenceSiroky, B. J., N. K. Kleene, S. J. Kleene, C. D. Jr Varnell, R. G. Comer, J. Liu, et al. 2017a. Primary cilia regulate the osmotic stress response of renal epithelial cells through TRPM3. Am. J. Physiol. Renal Physiol. 312: F791 – F805.
dc.identifier.citedreferenceSiroky, B. J., A. J. Towbin, A. T. Trout, H. Schafer, A. R. Thamann, K. D. Agricola, et al. 2017b. Improvement in renal cystic disease of tuberous sclerosis complex after treatment with mammalian target of rapamycin inhibitor. J. Pediatr. 187: 318 – 322 e312.
dc.identifier.citedreferenceSnippert, H. J., L. G. van der Flier, T. Sato, J. H. van Es, M. van den Born, C. Kroon‐Veenboer, et al. 2010. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143: 134 – 144.
dc.identifier.citedreferenceStillwell, T. J., M. R. Gomez, and P. P. Kelalis. 1987. Renal lesions in tuberous sclerosis. J. Urol. 138: 477 – 481.
dc.identifier.citedreferenceStoos, B. A., A. Náray‐Fejes‐Tóth, O. A. Carretero, S. Ito, and G. Fejes‐Tóth. 1991. Characterization of a mouse cortical collecting duct cell line. Kidney Int. 39: 1168 – 1175.
dc.identifier.citedreferenceSullivan, L. P., D. P. Wallace, and J. J. Grantham. 1998. Epithelial transport in polycystic kidney disease. Physiol. Rev. 78: 1165 – 1191.
dc.identifier.citedreferenceTeam RC. R: A language and environment for statistical computing R Foundation for Statistical Computing. 2018. http://www.R-project.org/.
dc.identifier.citedreferenceTherneau, T. 2018. A Package for Survival Analysis in S. version 2.38. https://CRAN.R-project.org/package=survival.
dc.identifier.citedreferenceTherneau, T. M., and P. M. Grambsch. 2000. P. 350 Modeling Survival Data: extending the Cox Model. Springer‐Verlag, New York.
dc.identifier.citedreferenceTraykova‐Brauch, M., K. Schonig, O. Greiner, T. Miloud, A. Jauch, M. Bode, et al. 2008. An efficient and versatile system for acute and chronic modulation of renal tubular function in transgenic mice. Nat. Med. 14: 979 – 984.
dc.identifier.citedreferenceVarasteh Kia, M., S. Barone, A. A. McDonough, K. Zahedi, J. Xu, and M. Soleimani. 2018. Downregulation of the Cl‐/HCO3‐exchanger pendrin in kidneys of mice with cystic fibrosis: role in the pathogenesis of metabolic alkalosis. Cell. Physiol. Biochem. 45: 1551 – 1565.
dc.identifier.citedreferenceWilson, C., C. Bonnet, C. Guy, S. Idziaszczyk, J. Colley, V. Humphreys, et al. 2006. Tsc1 haploinsufficiency without mammalian target of rapamycin activation is sufficient for renal cyst formation in Tsc1 + /‐ mice. Cancer Res. 66: 7934 – 7938.
dc.identifier.citedreferenceXu, J., S. Barone, H. Li, S. Holiday, K. Zahedi, and M. Soleimani. 2011. Slc26a11, a chloride transporter, localizes with the vacuolar H(+)‐ATPase of A‐intercalated cells of the kidney. Kidney Int. 80: 926 – 937.
dc.identifier.citedreferenceZahedi, K., S. Barone, J. Xu, and M. Soleimani. 2013. Potentiation of the effect of thiazide derivatives by carbonic anhydrase inhibitors: molecular mechanisms and potential clinical implications. PLoS ONE 8: e79327.
dc.identifier.citedreferenceZhou, J., J. Brugarolas, and L. F. Parada. 2009. Loss of Tsc1, but not Pten, in renal tubular cells causes polycystic kidney disease by activating mTORC1. Hum. Mol. Genet. 18: 4428 – 4441.
dc.identifier.citedreferenceZomer, A., C. Maynard, F. J. Verweij, A. Kamermans, R. Schafer, E. Beerling, et al. 2015. In Vivo imaging reveals extracellular vesicle‐mediated phenocopying of metastatic behavior. Cell 161: 1046 – 1057.
dc.identifier.citedreferenceZoncu, R., L. Bar‐Peled, A. Efeyan, S. Wang, Y. Sancak, and D. M. Sabatini. 2011. mTORC1 senses lysosomal amino acids through an inside‐out mechanism that requires the vacuolar H(+)‐ATPase. Science 334: 678 – 683.
dc.identifier.citedreferenceArmour, E. A., R. P. Carson, and K. C. Ess. 2012. Cystogenesis and elongated primary cilia in Tsc1‐deficient distal convoluted tubules. Am. J. Physiol. Renal Physiol. 303: F584 – F592.
dc.identifier.citedreferenceDoench, J. G., E. Hartenian, D. B. Graham, Z. Tothova, M. Hegde, I. Smith, et al. 2014. Rational design of highly active sgRNAs for CRISPR‐Cas9‐mediated gene inactivation. Nat. Biotechnol. 32: 1262 – 1267.
dc.identifier.citedreferenceArulrajah, S., G. Ertan, L. Jordan, A. Tekes, E. Khaykin, I. Izbudak, et al. 2009. Magnetic resonance imaging and diffusion‐weighted imaging of normal‐appearing white matter in children and young adults with tuberous sclerosis complex. Neuroradiology 51: 781 – 786.
dc.identifier.citedreferenceBadenas, C., R. Torra, L. Perez‐Oller, J. Mallolas, R. Talbot‐Wright, V. Torregrosa, et al. 2000. Loss of heterozygosity in renal and hepatic epithelial cystic cells from ADPKD1 patients. Eur. J. Hum. Genet. 8: 487 – 492.
dc.identifier.citedreferenceBarone, S., J. Xu, K. Zahedi, M. Brooks, and M. Soleimani. 2018. Probenecid pre‐treatment downregulates the kidney Cl(‐)/HCO3(‐) exchanger (pendrin) and potentiates hydrochlorothiazide‐induced diuresis. Front. Physiol. 9: 849.
dc.identifier.citedreferenceBenvenuto, G., S. Li, S. J. Brown, R. Braverman, W. C. Vass, J. P. Cheadle, et al. 2000. The tuberous sclerosis‐1 (TSC1) gene product hamartin suppresses cell growth and augments the expression of the TSC2 product tuberin by inhibiting its ubiquitination. Oncogene 19: 6306 – 6316.
dc.identifier.citedreferenceBissler, J. J. 2018. Cystic Kidney Diseases Associated with Increased Cancer Risk: tuberous Sclerosis Complex, Von Hippel Lindau, and Birt Hogg Dubé. Pp. 51 – 66 in B. D. Cowley Jr and J. J. Bissler, eds. Polycystic Kidney Disease: translating Mechanisms into Therapy. Springer, New York.
dc.identifier.citedreferenceBissler, J. J., and J. C. Kingswood. 2016. Optimal treatment of tuberous sclerosis complex associated renal angiomyolipomata: a systematic review. Ther. Adv. Urol. 8: 279 – 290.
dc.identifier.citedreferenceBissler, J. J., and C. Kingswood. 2018. Renal manifestation of tuberous sclerosis complex. Am. J. Med. Genet. 178: 338 – 347.
dc.identifier.citedreferenceBissler, J. J., F. X. McCormack, L. R. Young, J. M. Elwing, G. Chuck, J. M. Leonard, et al. 2008. Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis. N. Engl. J. Med. 358: 140 – 151.
dc.identifier.citedreferenceBissler, J. J., J. C. Kingswood, E. Radzikowska, B. A. Zonnenberg, M. Frost, E. Belousova, et al. 2013. Everolimus for angiomyolipoma associated with tuberous sclerosis complex or sporadic lymphangioleiomyomatosis (EXIST‐2): a multicentre, randomised, double‐blind, placebo‐controlled trial. Lancet 381: 817 – 824.
dc.identifier.citedreferenceBlake‐Palmer, K. G., and F. E. Karet. 2009. Cellular physiology of the renal H+ATPase. Curr. Opin. Nephrol. Hypertens. 18: 433 – 438.
dc.identifier.citedreferenceBongaarts, A., K. Giannikou, R. J. Reinten, J. J. Anink, J. D. Mills, F. E. Jansen, et al. 2017. Subependymal giant cell astrocytomas in tuberous sclerosis complex have consistent TSC1/TSC2 biallelic inactivation, and no BRAF mutations. Oncotarget 8: 95516 – 95529.
dc.identifier.citedreferenceBonsib, S. M., C. Boils, N. Gokden, D. Grignon, X. Gu, J. P. Higgins, et al. 2016. Tuberous sclerosis complex: hamartin and tuberin expression in renal cysts and its discordant expression in renal neoplasms. Pathol. Res. Pract. 212: 972 – 979.
dc.identifier.citedreferenceBrasier, J. L., and E. P. Henske. 1997. 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. 99: 194 – 199.
dc.identifier.citedreferenceBreton, S., and D. Brown. 2013. Regulation of luminal acidification by the V‐ATPase. Physiology (Bethesda) 28: 318 – 329.
dc.identifier.citedreferenceBrook‐Carter, P. T., B. Peral, C. J. Ward, P. Thompson, J. Hughes, M. M. Maheshwar, et al. 1994. Deletion of the TSC2 and PKD1 genes associated with severe infantile polycystic kidney disease–a contiguous gene syndrome. Nat. Genet. 8: 328 – 332.
dc.identifier.citedreferenceBrown, D., T. G. Paunescu, S. Breton, and V. Marshansky. 2009. Regulation of the V‐ATPase in kidney epithelial cells: dual role in acid‐base homeostasis and vesicle trafficking. J. Exp. Biol. 212: 1762 – 1772.
dc.identifier.citedreferenceCai, S., J. I. Everitt, H. Kugo, J. Cook, E. Kleymenova, and C. L. Walker. 2003. Polycystic kidney disease as a result of loss of the tuberous sclerosis 2 tumor suppressor gene during development. Am. J. Pathol. 162: 457 – 468.
dc.identifier.citedreferenceCao, T., and Y. Feng. 2013. The (pro)renin receptor and body fluid homeostasis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 305: R104 – R106.
dc.identifier.citedreferenceCell_Signaling_Technology. 2018. https://www.cellsignal.com/products/primary-antibodies/tuberin-tsc2-antibody/3612. 2018 ].
dc.identifier.citedreferenceChen, Z., H. Dong, C. Jia, Q. Song, J. Chen, Y. Zhang, et al. 2014. Activation of mTORC1 in collecting ducts causes hyperkalemia. J. Am. Soc. Nephrol. 25: 534 – 545.
dc.identifier.citedreferenceCrambert, G. 2014. H‐K‐ATPase type 2: relevance for renal physiology and beyond. Am. J. Physiol. Renal Physiol. 306: F693 – F700.
dc.identifier.citedreferenceCrino, P. B., E. Aronica, G. Baltuch, and K. L. Nathanson. 2010. Biallelic TSC gene inactivation in tuberous sclerosis complex. Neurology 74: 1716 – 1723.
dc.identifier.citedreferenceDabora, S. L., S. Jozwiak, D. N. Franz, P. S. Roberts, A. Nieto, J. Chung, et al. 2001. Mutational analysis in a cohort of 224 tuberous sclerosis patients indicates increased severity of TSC2, compared with TSC1, disease in multiple organs. Am. J. Hum. Genet. 68: 64 – 80.
dc.identifier.citedreferenceDanser, A. H. 2015. The role of the (Pro)renin receptor in hypertensive disease. Am. J. Hypertens. 28: 1187 – 1196.
dc.identifier.citedreferenceDodd, K. M., J. Yang, M. H. Shen, J. R. Sampson, and A. R. Tee. 2015. mTORC1 drives HIF‐1alpha and VEGF‐A signalling via multiple mechanisms involving 4E‐BP1, S6K1 and STAT3. Oncogene 34: 2239 – 2250.
dc.identifier.citedreferenceDoench, J. G., N. Fusi, M. Sullender, M. Hegde, E. W. Vaimberg, K. F. Donovan, et al. 2016. Optimized sgRNA design to maximize activity and minimize off‐target effects of CRISPR‐Cas9. Nat. Biotechnol. 34: 184 – 191.
dc.identifier.citedreferenceDziedzic, K., O. Pleniceanu, and B. Dekel. 2014. Kidney stem cells in development, regeneration and cancer. Semin. Cell Dev. Biol. 36: 57 – 65.
dc.identifier.citedreferenceElorza, A., I. Soro‐Arnaiz, F. Melendez‐Rodriguez, V. Rodriguez‐Vaello, G. Marsboom, G. de Carcer, et al. 2012. HIF2alpha acts as an mTORC1 activator through the amino acid carrier SLC7A5. Mol. Cell 48: 681 – 691.
dc.identifier.citedreferenceErtan, G., S. Arulrajah, A. Tekes, L. Jordan, and T. A. Huisman. 2010. Cerebellar abnormality in children and young adults with tuberous sclerosis complex: MR and diffusion weighted imaging findings. J. Neuroradiol. 37: 231 – 238.
dc.identifier.citedreferenceEwalt, D. H., E. Sheffield, S. P. Sparagana, M. R. Delgado, and E. S. Roach. 1998. Renal lesion growth in children with tuberous sclerosis complex. J. Urol. 160: 141 – 145.
dc.identifier.citedreferenceFernandez, R., J. R. Bosqueiro, A. C. Cassola, and G. Malnic. 1997. Role of Cl‐ in electrogenic H+ secretion by cortical distal tubule. J. Membr. Biol. 157: 193 – 201.
dc.identifier.citedreferenceFranz, D. N. 2013. Everolimus in the treatment of subependymal giant cell astrocytomas, angiomyolipomas, and pulmonary and skin lesions associated with tuberous sclerosis complex. Biologics 7: 211 – 221.
dc.identifier.citedreferenceFranz, D. N., K. Budde, J. C. Kingswood, E. Belousova, S. Sparagana, P. J. de Vries, et al. 2018. Effect of everolimus on skin lesions in patients treated for subependymal giant cell astrocytoma and renal angiomyolipoma: final 4‐year results from the randomised EXIST‐1 and EXIST‐2 studies. J. Eur. Acad. Dermatol. Venereol. 10: 1796 – 1803.
dc.identifier.citedreferenceGennari, F. J. 2011. Pathophysiology of metabolic alkalosis: a new classification based on the centrality of stimulated collecting duct ion transport. Am. J. Kidney Dis. 58: 626 – 636.
dc.identifier.citedreferenceGlenn, S. T., C. A. Jones, L. Pan, and K. W. Gross. 2008. In vivo analysis of key elements within the renin regulatory region. Physiol. Genomics 35: 243 – 253.
dc.identifier.citedreferenceGrantham, J. J. 2015. Rationale for early treatment of polycystic kidney disease. Pediatr. Nephrol. 30: 1053 – 1062.
dc.identifier.citedreferenceGrantham, J. J., J. L. Geiser, and A. P. Evan. 1987. Cyst formation and growth in autosomal dominant polycystic kidney disease. Kidney Int. 31: 1145 – 1152.
dc.identifier.citedreferenceHarris, P. C. 2002. Molecular basis of polycystic kidney disease: PKD1, PKD2 and PKHD1. Curr. Opin. Nephrol. Hypertens. 11: 309 – 314.
dc.identifier.citedreferenceHasumi, Y., M. Baba, R. Ajima, H. Hasumi, V. A. Valera, M. E. Klein, et al. 2009. Homozygous loss of BHD causes early embryonic lethality and kidney tumor development with activation of mTORC1 and mTORC2. Proc. Natl. Acad. Sci. U S A 106: 18722 – 18727.
dc.identifier.citedreferenceHenske, E. P., H. P. Neumann, B. W. Scheithauer, E. W. Herbst, M. P. Short, and D. J. Kwiatkowski. 1995. Loss of heterozygosity in the tuberous sclerosis (TSC2) region of chromosome band 16p13 occurs in sporadic as well as TSC‐associated renal angiomyolipomas. Genes Chromosom. Cancer 13: 295 – 298.
dc.identifier.citedreferenceHenske, E. P., B. W. Scheithauer, M. P. Short, R. Wollmann, J. Nahmias, N. Hornigold, et al. 1996. Allelic loss is frequent in tuberous sclerosis kidney lesions but rare in brain lesions. Am. J. Hum. Genet. 59: 400 – 406.
dc.identifier.citedreferenceHogan, M. C., L. Manganelli, J. R. Woollard, A. I. Masyuk, T. V. Masyuk, R. Tammachote, et al. 2009. Characterization of PKD protein‐positive exosome‐like vesicles. J. Am. Soc. Nephrol. 20: 278 – 288.
dc.identifier.citedreferenceHsu, P. D., D. A. Scott, J. A. Weinstein, F. A. Ran, S. Konermann, V. Agarwala, et al. 2013. DNA targeting specificity of RNA‐guided Cas9 nucleases. Nat. Biotechnol. 31: 827 – 832.
dc.identifier.citedreferenceJanicke, M., T. J. Carney, and M. Hammerschmidt. 2007. Foxi3 transcription factors and Notch signaling control the formation of skin ionocytes from epidermal precursors of the zebrafish embryo. Dev. Biol. 307: 258 – 271.
dc.identifier.citedreferenceJones, A. C., C. E. Daniells, R. G. Snell, M. Tachataki, S. A. Idziaszczyk, M. Krawczak, et al. 1997. Molecular genetic and phenotypic analysis reveals differences between TSC1 and TSC2 associated familial and sporadic tuberous sclerosis. Hum. Mol. Genet. 6: 2155 – 2161.
dc.identifier.citedreferenceJulian, L. M., and W. L. Stanford. 2017. Reprogramming patient‐derived tumor cells generates model cell lines for tuberous sclerosis‐associated lymphangioleiomyomatosis. Oncoscience 4: 170 – 172.
dc.identifier.citedreferenceJurkiewicz, E., S. Jozwiak, M. Bekiesinska‐Figatowska, and J. Walecki. 2007. Apparent diffusion coefficient is increased in children with tuberous sclerosis complex personal experience and review of the literature. Neuroradiol. J. 20: 622 – 626.
dc.identifier.citedreferenceKanemoto, S., R. Nitani, T. Murakami, M. Kaneko, R. Asada, K. Matsuhisa, et al. 2016. Multivesicular body formation enhancement and exosome release during endoplasmic reticulum stress. Biochem. Biophys. Res. Commun. 480: 166 – 172.
dc.identifier.citedreferenceKaneshiro, Y., A. Ichihara, T. Takemitsu, M. Sakoda, F. Suzuki, T. Nakagawa, et al. 2006. Increased expression of cyclooxygenase‐2 in the renal cortex of human prorenin receptor gene‐transgenic rats. Kidney Int. 70: 641 – 646.
dc.identifier.citedreferenceKim, J., and E. Kim. 2016. Rag GTPase in amino acid signaling. Amino Acids 48: 915 – 928.
dc.identifier.citedreferenceKim, H., H. Xu, Q. Yao, W. Li, Q. Huang, P. Outeda, et al. 2014. Ciliary membrane proteins traffic through the Golgi via a Rabep1/GGA1/Arl3‐dependent mechanism. Nat. Commun. 5: 5482.
dc.identifier.citedreferenceKing, H. W., M. Z. Michael, and J. M. Gleadle. 2012. Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 12: 421.
dc.identifier.citedreferenceKwiatkowski, D. J., H. Zhang, J. L. Bandura, K. M. Heiberger, M. Glogauer, N. el‐Hashemite, et al. 2002. A mouse model of TSC1 reveals sex‐dependent lethality from liver hemangiomas, and up‐regulation of p70S6 kinase activity in Tsc1 null cells. Hum. Mol. Genet. 11: 525 – 534.
dc.identifier.citedreferenceLam, H. C., J. Nijmeh, and E. P. Henske. 2017. New developments in the genetics and pathogenesis of tumours in tuberous sclerosis complex. J. Pathol. 241: 219 – 225.
dc.identifier.citedreferenceLee, B. S. 2012. Regulation of V‐ATPase expression in mammalian cells. Curr. Protein Pept. Sci. 13: 107 – 116.
dc.identifier.citedreferencede Lemos Barbosa, C. M., J. Souza‐Menezes, A. G. Amaral, L. F. Onuchic, L. Cebotaru, W. B. Guggino, et al. 2016. Regulation of CFTR expression and arginine vasopressin activity are dependent on polycystin‐1 in kidney‐derived cells. Cell. Physiol. Biochem. 38: 28 – 39.
dc.identifier.citedreferenceMaas, S. L. N., X. O. Breakefield, and A. M. Weaver. 2017. Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol. 27: 172 – 188.
dc.identifier.citedreferenceMcCormack, F. X., Y. Inoue, J. Moss, L. G. Singer, C. Strange, K. Nakata, et al. 2011. Efficacy and safety of sirolimus in lymphangioleiomyomatosis. N. Engl. J. Med. 364: 1595 – 1606.
dc.identifier.citedreferenceNomura, S., M. Kaminishi, N. Takagi, and H. Esumi. 2004. Analysis of promoter region of X‐linked pgk‐1 gene polymorphisms: evidence for polyclonality of adult mouse gastric glands. Dig Dis Sci. 49: 218 – 23.
dc.identifier.citedreferenceOnda, H., A. Lueck, P. W. Marks, H. B. Warren, and D. J. Kwiatkowski. 1999. Tsc2(+/‐) mice develop tumors in multiple sites that express gelsolin and are influenced by genetic background. J. Clin. Invest. 104: 687 – 695.
dc.identifier.citedreferenceParolini, I., C. Federici, C. Raggi, L. Lugini, S. Palleschi, A. De Milito, et al. 2009. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J. Biol. Chem. 284: 34211 – 34222.
dc.identifier.citedreferenceParry, L., J. H. Maynard, A. Patel, A. K. Hodges, A. von Deimling, J. R. Sampson, et al. 2000. Molecular analysis of the TSC1 and TSC2 tumour suppressor genes in sporadic glial and glioneuronal tumours. Hum. Genet. 107: 350 – 356.
dc.identifier.citedreferencePatel, B., J. Patel, J. H. Cho, S. Manne, S. Bonala, E. Henske, et al. 2016. Exosomes mediate the acquisition of the disease phenotypes by cells with normal genome in tuberous sclerosis complex. Oncogene 35: 3027 – 3036.
dc.identifier.citedreferencePema, M., L. Drusian, M. Chiaravalli, M. Castelli, Q. Yao, S. Ricciardi, et al. 2016. mTORC1‐mediated inhibition of polycystin‐1 expression drives renal cyst formation in tuberous sclerosis complex. Nat. Commun. 7: 10786.
dc.identifier.citedreferencePena‐Llopis, S., and J. Brugarolas. 2011. TFEB, a novel mTORC1 effector implicated in lysosome biogenesis, endocytosis and autophagy. Cell Cycle 10: 3987 – 3988.
dc.identifier.citedreferencePena‐Llopis, S., S. Vega‐Rubin‐de‐Celis, J. C. Schwartz, N. C. Wolff, T. A. Tran, L. Zou, et al. 2011. Regulation of TFEB and V‐ATPases by mTORC1. EMBO J. 30: 3242 – 3258.
dc.identifier.citedreferencePeters, J. 2017. The (pro)renin receptor and its interaction partners. Pflugers Arch. 469: 1245 – 1256.
dc.identifier.citedreferencePomatto, M. A. C., C. Gai, B. Bussolati, and G. Camussi. 2017. Extracellular vesicles in renal pathophysiology. Front. Mol. Biosci. 4: 37.
dc.identifier.citedreferenceProteinTech. 2018. Tuberin‐Specific Antibody Catalog number: 20004‐1‐AP https://www.ptglab.com/products/TSC2-Specific-Antibody-20004-1-AP.htm#validation. 2018 ].
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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