Urine-sample-derived human induced pluripotent stem cells as a model to study PCSK9-mediated autosomal dominant hypercholesterolemia

DMM Disease Models and Mechanisms

Volumn 9, Issue 1, 2016, Pages 81-90

  Si Tayeb, Karim ^a,b   Idriss, Salam ^a,b,c,d   Champon, Benoite ^a,b   Caillaud, Amandine ^a,b   Pichelin, Matthieu ^a,b   Arnaud, Lucie ^a,b   Lemarchand, Patricia ^a,b   Le May, Cédric ^a,b   Zibara, Kazem ^c,d   Cariou, Bertrand ^a,b  

^a L INSTITUT DU THORAX   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c PRASE   (Lebanon)

^d LEBANESE UNIVERSITY   (Lebanon)

Author keywords

Autosomal dominant hypercholesterolemia; Hepatocyte differentiation; Human induced pluripotent stem cells; PCSK9; Urine derived somatic cells

Indexed keywords

LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; PEPTIDES AND PROTEINS; PRAVASTATIN; PROPROTEIN CONVERTASE SUBTILISIN KEXIN TYPE 9; UNCLASSIFIED DRUG; MESSENGER RNA; PCSK9 PROTEIN, HUMAN; PROPROTEIN CONVERTASE 9; SERINE PROTEINASE;

ADULT; AGED; ARTICLE; AUTOSOMAL DOMINANT HYPERCHOLESTEROLEMIA; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; FAMILIAL HYPOBETALIPOPROTEINEMIA; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPERCHOLESTEROLEMIA; LIVER CELL; MIDDLE AGED; NUCLEAR REPROGRAMMING; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN SECRETION; URINE SAMPLE DERIVED HUMAN INDUCED PLURIPOTENT STEM CELL; ANIMAL; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; FAMILIAL HYPERCHOLESTEROLEMIA; FIBROBLAST; GENE EXPRESSION PROFILING; GENETICS; INDUCED PLURIPOTENT STEM CELL; KARYOTYPING; MALE; METABOLISM; MOUSE; MUTATION; URINE;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHOLESTEROL, LDL; FEMALE; FIBROBLASTS; GENE EXPRESSION PROFILING; HEPATOCYTES; HUMANS; HYPERLIPOPROTEINEMIA TYPE II; INDUCED PLURIPOTENT STEM CELLS; KARYOTYPING; LIPOPROTEINS, LDL; MALE; MICE; MUTATION; PRAVASTATIN; PROPROTEIN CONVERTASE 9; PROPROTEIN CONVERTASES; RNA, MESSENGER; SERINE ENDOPEPTIDASES; URINE;

EID: 84954473216     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.022277     Document Type: Article

References (35)

1. Abifadel, M., Varret, M., Rabeìs, J.-P., Allard, D., Ouguerram, K., Devillers, M., Cruaud, C., Benjannet, S., Wickham, L., Erlich, D. et al. (2003). Mutations in PCSK9 cause autosomal dominant hypercholesterolemia. Nat. Genet. 34, 154-156.
2. Benjannet, S., Rhainds, D., Essalmani, R., Mayne, J., Wickham, L., Jin, W., Asselin, M.-C., Hamelin, J., Varret, M., Allard, D. et al. (2004). NARC-1/PCSK9 and its natural mutants: zymogen cleavage and effects on the low density lipoprotein (LDL) receptor and LDL cholesterol. J. Biol. Chem. 279, 48865-48875.
3. Berge, K. E., Ose, L. and Leren, T. P. (2006). Missense mutations in the PCSK9 gene are associated with hypocholesterolemia and possibly increased response to statin therapy. Arterioscler. Thromb. Vasc. Biol. 26, 1094-1100.
4. Bharadwaj, S., Liu, G., Shi, Y., Wu, R., Yang, B., He, T., Fan, Y., Lu, X., Zhou, X., Liu, H. et al. (2013). Multi-potential differentiation of human urine-derived stem cells: potential for therapeutic applications in urology. Stem Cells 31, 1840-1856.
5. Blom, D. J., Hala, T., Bolognese, M., Lillestol, M. J., Toth, P.D., Burgess, L., Ceska, R., Roth, E., Koren, M. J., Ballantyne, C. M. et al. (2014). A 52-week placebocontrolled trial of evolocumab in hyperlipidemia. N. Engl. J. Med. 370, 1809-1819.
6. Cameron, J., Holla, Ø. L., Ranheim, T., Kulseth, M. A., Berge, K. E. and Leren, T. P. (2006). Effect of mutations in the PCSK9 gene on the cell surface LDL receptors. Hum. Mol. Genet. 15, 1551-1558.
7. Cannon, C. P., Cariou, B., Blom, D., McKenney, J. M., Lorenzato, C., Pordy, R., Chaudhari, U. and Colhoun, H. M. (2015). Efficacy and safety of alirocumab in high cardiovascular risk patients with inadequately controlled hypercholesterolaemia on maximally tolerated doses of statins: the ODYSSEY COMBO II randomized controlled trial. Eur. Heart J. 36, 1186-1194.
8. Cariou, B., Ouguerram, K., Zair, Y., Guerois, R., Langhi, C., Kourimate, S., Benoit, I., Le May, C., Gayet, C., Belabbas, K. et al. (2009). PCSK9 dominant negative mutant results in increased LDL catabolic rate and familial hypobetalipoproteinemia. Arterioscler. Thromb. Vasc. Biol. 29, 2191-2197.
9. Cariou, B., Le May, C. and Costet, P. (2011). Clinical aspects of PCSK9. Atherosclerosis 216, 258-265.
10. Cayo, M. A., Cai, J., DeLaForest, A., Noto, F. K., Nagaoka, M., Clark, B. S., Collery, R. F., Si-Tayeb, K. and Duncan, S. A. (2012). JD induced pluripotent stem cell-derived hepatocytes faithfully recapitulate the pathophysiology of familial hypercholesterolemia. Hepatology 56, 2163-2171.
11. Cohen, J. C., Boerwinkle, E., Mosley, T. H. and Hobbs, H. H. (2006). Sequence variations in PCSK9, low LDL, and protection against coronary heart disease. N. Engl. J. Med. 354, 1264-1272.
12. Costet, P., Krempf, M. and Cariou, B. (2008). PCSK9 and LDL cholesterol: unravelling the target to design the bullet. Trends Biochem. Sci. 33, 426-434.
13. DeLaForest, A., Nagaoka, M., Si-Tayeb, K., Noto, F. K., Konopka, G., Battle, M. A. and Duncan, S. A. (2011). HNF4A is essential for specification of hepatic progenitors from human pluripotent stem cells. Development 138, 4143-4153.
14. Farnier, M. (2013). PCSK9 inhibitors. Curr. Opin. Lipidol. 24, 251-258.
15. Gerbal-Chaloin, S., Funakoshi, N., Caillaud, A., Gondeau, C., Champon, B. and Si-Tayeb, K. (2014). Human induced pluripotent stem cells in hepatology: beyond the proof of concept. Am. J. Pathol. 184, 332-347.
16. Holla, Ø. L., Cameron, J., Berge, K. E., Kulseth, M. A., Ranheim, T. and Leren, T. P. (2006). Low-density lipoprotein receptor activity in Epstein-Barr virustransformed lymphocytes from heterozygotes for the D374Y mutation in the PCSK9 gene. Scand. J. Clin. Lab. Invest. 66 317-328.
17. Idriss, S., Zibara, K., Cariou, B. and Si-Tayeb, K. (2015). From human-induced pluripotent stem cells to liver disease modeling: a focus on dyslipidemia. Curr. Pathobiol. Rep. 3, 47-56.
18. Jones, P., Kafonek, S., Laurora, I. and Hunninghake, D. (1998). Comparative dose efficacy study of atorvastatin versus simvastatin, pravastatin, lovastatin, and fluvastatin in patients with hypercholesterolemia (the CURVES study). Am. J. Cardiol. 81, 582-587.
19. Jones, P. H., Davidson, M. H., Stein, E. A., Bays, H. E., McKenney, J. M., Miller, E., Cain, V. A. and Blasetto, J. W. (2003). Comparison of the efficacy and safety of rosuvastatin versus atorvastatin, simvastatin, and pravastatin across doses (STELLAR∗Trial). Am. J. Cardiol. 92, 152-160.
20. Lang, R., Liu, G., Shi, Y., Bharadwaj, S., Leng, X., Zhou, X., Liu, H., Atala, A. and Zhang, Y. (2013). Self-renewal and differentiation capacity of urine-derived stem cells after urine preservation for 24 hours. PLoS ONE 8, e53980. .
21. Miranda, M. X., van Tits, L. J., Lohmann, C., Arsiwala, T., Winnik, S., Tailleux, A., Stein, S., Gomes, A. P., Suri, V., Ellis, J. L. et al. (2015). The Sirt1 activator SRT3025 provides atheroprotection in Apoe-/- mice by reducing hepatic Pcsk9 secretion and enhancing Ldlr expression. Eur. Heart J. 36, 51-59.
22. Pandit, S., Wisniewski, D., Santoro, J. C., Ha, S., Ramakrishnan, V., Cubbon, R. M., Cummings, R. T., Wright, S. D., Sparrow, C. P., Sitlani, A. et al. (2008). Functional analysis of sites within PCSK9 responsible for hypercholesterolemia. J. Lipid Res. 49, 1333-1343.
23. Park, S.W., Moon, Y.-A. and Horton, J. D. (2004). Post-transcriptional regulation of low density lipoprotein receptor protein by proprotein convertase subtilisin/kexin type 9a in mouse liver. J. Biol. Chem. 279, 50630-50638.
24. Rashid, S., Curtis, D. E., Garuti, R., Anderson, N. N., Bashmakov, Y., Ho, Y. K., Hammer, R. E., Moon, Y.-A. and Horton, J. D. (2005). Decreased plasma cholesterol and hypersensitivity to statins in mice lacking Pcsk9. Proc. Natl. Acad. Sci. USA 102, 5374-5379.
25. Rashid, S. T., Corbineau, S., Hannan, N., Marciniak, S. J., Miranda, E., Alexander, G., Huang-Doran, I., Griffin, J., Ahrlund-Richter, L., Skepper, J. et al. (2010). Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J. Clin. Invest. 120, 3127-3136.
26. Romagnuolo, R., Scipione, C. A., Boffa, M. B., Marcovina, S. M., Seidah, N. G. and Koschinsky, M. L. (2015). Lipoprotein (a) catabolism is regulated by Proprotein Convertase Subtilisin/Kexin type 9 through the low density lipoprotein receptor. J. Biol. Chem. 290, 11649-11662.
27. Roth, E. M. and Diller, P. (2014). Alirocumab for hyperlipidemia: physiology of PCSK9 inhibition, pharmacodynamics and Phase I and II clinical trial results of a PCSK9 monoclonal antibody. Future Cardiol. 10, 183-199.
28. Seidah, N. G., Benjannet, S., Wickham, L., Marcinkiewicz, J., Jasmin, S. B., Stifani, S., Basak, A., Prat, A. and Chretien, M. (2003). The secretory proprotein convertase neural apoptosis-regulated convertase 1 (NARC-1): liver regeneration and neuronal differentiation. Proc. Natl. Acad. Sci. USA 100, 928-933.
29. Seidah, N. G., Awan, Z., Chretien, M. and Mbikay, M. (2014). PCSK9: a key modulator of cardiovascular health. Circ. Res. 114, 1022-1036.
30. Si-Tayeb, K., Noto, F. K., Nagaoka, M., Li, J., Battle, M. A., Duris, C., North, P. E., Dalton, S. and Duncan, S. A. (2010). Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 51, 297-305.
31. Sniderman, A. D., Qi, Y., Ma, C.-I. J., Wang, R. H. L., Naples, M., Baker, C., Zhang, J., Adeli, K. and Kiss, R. S. (2013). Hepatic cholesterol homeostasis: is the low-density lipoprotein pathway a regulatory or a shunt pathway? Arterioscler. Thromb. Vasc. Biol. 33, 2481-2490.
32. Sun, X.-M., Eden, E. R., Tosi, I., Neuwirth, C. K., Wile, D., Naoumova, R. P. and Soutar, A. K. (2005). Evidence for effect of mutant PCSK9 on apolipoprotein B secretion as the cause of unusually severe dominant hypercholesterolaemia. Hum. Mol. Genet. 14, 1161-1169.
33. Xue, Y., Cai, X., Wang, L., Liao, B., Zhang, H., Shan, Y., Chen, Q., Zhou, T., Li, X., Hou, J. et al. (2013). Generating a non-integrating human induced pluripotent stem cell bank from urine-derived cells. PLoS ONE 8, e70573.
34. Zaid, A., Roubtsova, A., Essalmani, R., Marcinkiewicz, J., Chamberland, A., Hamelin, J., Tremblay, M., Jacques, H., Jin, W., Davignon, J. et al. (2008). Proprotein convertase subtilisin/kexin type 9 (PCSK9): hepatocyte-specific lowdensity lipoprotein receptor degradation and critical role in mouse liver regeneration. Hepatology 48, 646-654.
35. Zhou, T., Benda, C., Dunzinger, S., Huang, Y., Ho, J. C., Yang, J., Wang, Y., Zhang, Y., Zhuang, Q., Li, Y. et al. (2012). Generation of human induced pluripotent stem cells from urine samples. Nat. Protoc. 7, 2080-2089.