Functions of Huntingtin in Germ Layer Specification and Organogenesis

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Nguyen, Giang D ^a   Molero, Aldrin E ^a   Gokhan, Solen ^a   Mehler, Mark F ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUNTINGTIN; NOTCH RECEPTOR; PROTEIN BAX; RETINOIC ACID; STAT2 PROTEIN; TRANSCRIPTION FACTOR HES 1; WNT3A PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DEVELOPMENTAL STAGE; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYOID BODY; EMBRYONIC STEM CELL; GERM CELL; HEART MUSCLE CELL; LIVER CELL; MESODERM; MOLECULAR PATHOLOGY; MOUSE; NERVE CELL; NONHUMAN; ORGANOGENESIS; PANCREAS CELL; PROTEIN EXPRESSION;

ANIMALS; CELL DIFFERENTIATION; ECTODERM; EMBRYOID BODIES; EMBRYONIC STEM CELLS; ENDODERM; GENE KNOCKOUT TECHNIQUES; GERM LAYERS; MESODERM; MICE; MUTATION; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; NUCLEAR PROTEINS; OLIGODENDROGLIA; ORGANOGENESIS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84881539152     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072698     Document Type: Article

References (80)

1. Gil JM, Rego AC, (2008) Mechanisms of neurodegeneration in Huntington's disease. Eur J Neurosci 27: 2803-2820. doi:10.1111/j.1460-9568.2008.06310.x. PubMed: 18588526.
2. Harjes P, Wanker EE, (2003) The hunt for huntingtin function: interaction partners tell many different stories. Trends Biochem Sci 28: 425-433. doi:10.1016/S0968-0004(03)00168-3. PubMed: 12932731.
3. Cattaneo E, Zuccato C, Tartari M, (2005) Normal huntingtin function: an alternative approach to Huntington's disease. Nat Rev Neurosci 6: 919-930. doi:10.1038/nrm1782. PubMed: 16288298.
4. Zuccato C, Valenza M, Cattaneo E, (2010) Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol Rev 90: 905-981. doi:10.1152/physrev.00041.2009. PubMed: 20664076.
5. Zeitlin S, Liu JP, Chapman DL, Papaioannou VE, Efstratiadis A, (1995) Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington's disease gene homologue. Nat Genet 11: 155-163. doi:10.1038/ng1095-155. PubMed: 7550343.
6. Woda JM, Calzonetti T, Hilditch-Maguire P, Duyao MP, Conlon RA, et al. (2005) Inactivation of the Huntington's disease gene (Hdh) impairs anterior streak formation and early patterning of the mouse embryo. BMC Dev Biol 5: 17. doi:10.1186/1471-213X-5-17. PubMed: 16109169.
7. Duyao MP, Auerbach AB, Ryan A, Persichetti F, Barnes GT, et al. (1995) Inactivation of the mouse Huntington's disease gene homolog Hdh. Science 269: 407-410. doi:10.1126/science.7618107. PubMed: 7618107.
8. Nasir J, Floresco SB, O'Kusky JR, Diewert VM, Richman JM, et al. (1995) Targeted disruption of the Huntington's disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell 81: 811-823. doi:10.1016/0092-8674(95)90542-1. PubMed: 7774020.
9. Godin JD, Colombo K, Molina-Calavita M, Keryer G, Zala D, et al. (2010) Huntingtin is required for mitotic spindle orientation and mammalian neurogenesis. Neuron 67: 392-406. doi:10.1016/j.neuron.2010.06.027. PubMed: 20696378.
10. Reiner A, Del Mar N, Meade CA, Yang H, Dragatsis I, et al. (2001) Neurons lacking huntingtin differentially colonize brain and survive in chimeric mice. J Neurosci 21: 7608-7619. PubMed: 11567051.
11. Molero AE, Gokhan S, Gonzalez S, Feig JL, Alexandre LC, et al. (2009) Impairment of developmental stem cell-mediated striatal neurogenesis and pluripotency genes in a knock-in model of Huntington's disease. Proc Natl Acad Sci U S A 106: 21900-21905. doi:10.1073/pnas.0912171106. PubMed: 19955426.
12. Carter RL, Chan AW, (2012) Pluripotent stem cells models for Huntington's disease: prospects and challenges. J Genet Genomics = Yi Chuan Xue Bao 39: 253-259. doi:10.1016/j.jgg.2012.04.006. PubMed: 22749012.
13. Yeo JC, Ng HH, (2013) The transcriptional regulation of pluripotency. Cell Res 23: 20-32. doi:10.1038/cr.2012.172. PubMed: 23229513.
14. MacDonald ME, Duyao M, Calzonetti T, Auerbach A, Ryan A, et al. (1996) Targeted inactivation of the mouse Huntington's disease gene homolog Hdh. Cold Spring Harb Symp Quant Biol 61: 627-638. doi:10.1101/SQB.1996.061.01.063. PubMed: 9246489.
15. Conforti P, Camnasio S, Mutti C, Valenza M, Thompson M, et al. (2013) Lack of huntingtin promotes neural stem cells differentiation into glial cells while neurons expressing huntingtin with expanded polyglutamine tracts undergo cell death. Neurobiol Dis 50: 160-170. doi:10.1016/j.nbd.2012.10.015. PubMed: 23089356.
16. Wheeler VC, Auerbach W, White JK, Srinidhi J, Auerbach A, et al. (1999) Length-dependent gametic CAG repeat instability in the Huntington's disease knock-in mouse. Hum Mol Genet 8: 115-122. doi:10.1093/hmg/8.1.115. PubMed: 9887339.
17. Hirai H, Karian P, Kikyo N, (2011) Regulation of embryonic stem cell self-renewal and pluripotency by leukaemia inhibitory factor. Biochem J 438: 11-23. doi:10.1042/BJ20102152. PubMed: 21793804.
18. Guan K, Rohwedel J, Wobus AM, (1999) Embryonic stem cell differentiation models: cardiogenesis, myogenesis, neurogenesis, epithelial and vascular smooth muscle cell differentiation in vitro. Cytotechnology 30: 211-226. doi:10.1023/A:1008041420166. PubMed: 19003371.
19. Zhang Y, Leavitt BR, van Raamsdonk JM, Dragatsis I, Goldowitz D, et al. (2006) Huntingtin inhibits caspase-3 activation. EMBO J 25: 5896-5906. doi:10.1038/sj.emboj.7601445. PubMed: 17124493.
20. Rigamonti D, Sipione S, Goffredo D, Zuccato C, Fossale E, et al. (2001) Huntingtin's neuroprotective activity occurs via inhibition of procaspase-9 processing. J Biol Chem 276: 14545-14548. doi:10.1074/jbc.C100044200. PubMed: 11278258.
21. Arnold SJ, Robertson EJ, (2009) Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 10: 91-103. doi:10.1038/nrm2618. PubMed: 19129791.
22. Thomson M, Liu SJ, Zou LN, Smith Z, Meissner A, et al. (2011) Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell 145: 875-889. doi:10.1016/j.cell.2011.05.017. PubMed: 21663792.
23. Schroeder IS, Rolletschek A, Blyszczuk P, Kania G, Wobus AM, (2006) Differentiation of mouse embryonic stem cells to insulin-producing cells. Nat Protoc 1: 495-507. doi:10.1038/nprot.2006.71. PubMed: 17406275.
24. Zaret KS, (2001) Hepatocyte differentiation: from the endoderm and beyond. Curr Opin Genet Dev 11: 568-574. doi:10.1016/S0959-437X(00)00234-3. PubMed: 11532400.
25. Hamazaki T, Iiboshi Y, Oka M, Papst PJ, Meacham AM, et al. (2001) Hepatic maturation in differentiating embryonic stem cells in vitro. FEBS Lett 497: 15-19. doi:10.1016/S0014-5793(01)02423-1. PubMed: 11376655.
26. Fässler R, Rohwedel J, Maltsev V, Bloch W, Lentini S, et al. (1996) Differentiation and integrity of cardiac muscle cells are impaired in the absence of beta 1 integrin. J Cell Sci 109(13):: 2989-2999. PubMed: 9004034.
27. Chiba S, (2006) Notch signaling in stem cell systems. Stem Cells 24: 2437-2447. doi:10.1634/stemcells.2005-0661. PubMed: 16888285.
28. Kageyama R, Ohtsuka T, Kobayashi T, (2007) The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 134: 1243-1251. doi:10.1242/dev.000786. PubMed: 17329370.
29. Kamakura S, Oishi K, Yoshimatsu T, Nakafuku M, Masuyama N, et al. (2004) Hes binding to STAT3 mediates crosstalk between Notch and JAK-STAT signalling. Nat Cell Biol 6: 547-554. doi:10.1038/ncb1138. PubMed: 15156153.
30. Nguyen GD, [!(surname)!], Molero AE, Mehler MF, (2013) Selective roles of normal and mutant huntingtin in neural induction and early neurogenesis. PLOS ONE 8(5):: e64368. doi:10.1371/journal.pone.0064368. PubMed: 23691206.
31. Ritch JJ, Valencia A, Alexander J, Sapp E, Gatune L, et al. (2012) Multiple phenotypes in Huntington disease mouse neural stem cells. Mol Cell Neurosci 50: 70-81. doi:10.1016/j.mcn.2012.03.011. PubMed: 22508027.
32. Hackam AS, Yassa AS, Singaraja R, Metzler M, Gutekunst CA, et al. (2000) Huntingtin interacting protein 1 induces apoptosis via a novel caspase-dependent death effector domain. J Biol Chem 275: 41299-41308. doi:10.1074/jbc.M008408200. PubMed: 11007801.
33. Gervais FG, Singaraja R, Xanthoudakis S, Gutekunst CA, Leavitt BR, et al. (2002) Recruitment and activation of caspase-8 by the Huntingtin-interacting protein Hip-1 and a novel partner Hippi. Nat Cell Biol 4: 95-105. doi:10.1038/ncb735. PubMed: 11788820.
34. Lo Sardo V, Zuccato C, Gaudenzi G, Vitali B, Ramos C, et al. (2012) An evolutionary recent neuroepithelial cell adhesion function of huntingtin implicates ADAM10-Ncadherin. Nat Neurosci 15: 713-721. doi:10.1038/nn.3080. PubMed: 22466506.
35. Almeida S, Sarmento-Ribeiro AB, Januário C, Rego AC, Oliveira CR, (2008) Evidence of apoptosis and mitochondrial abnormalities in peripheral blood cells of Huntington's disease patients. Biochem Biophys Res Commun 374: 599-603. doi:10.1016/j.bbrc.2008.07.009. PubMed: 18625199.
36. Luo S, Rubinsztein DC, (2009) Huntingtin promotes cell survival by preventing Pak2 cleavage. J Cell Sci 122: 875-885. doi:10.1242/jcs.050013. PubMed: 19240112.
37. de la Pompa JL, Epstein JA, (2012) Coordinating tissue interactions: Notch signaling in cardiac development and disease. Dev Cell 22: 244-254. doi:10.1016/j.devcel.2012.01.014. PubMed: 22340493.
38. Wang T, You N, Tao K, Wang X, Zhao G, et al. (2012) Notch is the key factor in the process of fetal liver stem/progenitor cells differentiation into hepatocytes. Dev Growth Differ 54: 605-617. doi:10.1111/j.1440-169X.2012.01363.x. PubMed: 22680933.
39. Ninov N, Borius M, Stainier DY, (2012) Different levels of Notch signaling regulate quiescence, renewal and differentiation in pancreatic endocrine progenitors. Development 139: 1557-1567. doi:10.1242/dev.076000. PubMed: 22492351.
40. Shimojo H, Ohtsuka T, Kageyama R, (2011) Dynamic expression of notch signaling genes in neural stem/progenitor cells. Front Neurosci 5: 78. PubMed: 21716644.
41. Moores JN, Roy S, Nicholson DW, Staveley BE, (2008) Huntingtin interacting protein 1 can regulate neurogenesis in Drosophila. Eur J Neurosci 28: 599-609. doi:10.1111/j.1460-9568.2008.06359.x. PubMed: 18702731.
42. Godin JD, Poizat G, Hickey MA, Maschat F, Humbert S, (2010) Mutant huntingtin-impaired degradation of beta-catenin causes neurotoxicity in Huntington's disease. EMBO J 29: 2433-2445. doi:10.1038/emboj.2010.117. PubMed: 20531388.
43. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, et al. (1999) Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22: 361-365. doi:10.1038/11932. PubMed: 10431240.
44. Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, et al. (1995) Lack of beta-catenin affects mouse development at gastrulation. Development 121: 3529-3537. PubMed: 8582267.
45. Zuccato C, Tartari M, Crotti A, Goffredo D, Valenza M, et al. (2003) Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat Genet 35: 76-83. doi:10.1038/ng1219. PubMed: 12881722.
46. Yamada Y, Aoki H, Kunisada T, Hara A, (2010) Rest promotes the early differentiation of mouse ESCs but is not required for their maintenance. Cell Stem Cell 6: 10-15. doi:10.1016/j.stem.2009.12.003. PubMed: 20085738.
47. Pfendler KC, Catuar CS, Meneses JJ, Pedersen RA, (2005) Overexpression of Nodal promotes differentiation of mouse embryonic stem cells into mesoderm and endoderm at the expense of neuroectoderm formation. Stem Cells Dev 14: 162-172. doi:10.1089/scd.2005.14.162. PubMed: 15910242.
48. Myers RH, Vonsattel JP, Paskevich PA, Kiely DK, Stevens TJ, et al. (1991) Decreased neuronal and increased oligodendroglial densities in Huntington's disease caudate nucleus. J Neuropathol Exp Neurol 50: 729-742. doi:10.1097/00005072-199111000-00005. PubMed: 1836225.
49. Younes L, Ratnanather JT, Brown T, Aylward E, Nopoulos P, et al. (2012) Regionally selective atrophy of subcortical structures in prodromal HD as revealed by statistical shape analysis. Hum: Brain Mapp.
50. Ciarmiello A, Cannella M, Lastoria S, Simonelli M, Frati L, et al. (2006) Brain white-matter volume loss and glucose hypometabolism precede the clinical symptoms of Huntington's disease. J Nucl Med 47: 215-222. PubMed: 16455626.
51. Paulsen JS, Nopoulos PC, Aylward E, Ross CA, Johnson H, et al. (2010) Striatal and white matter predictors of estimated diagnosis for Huntington disease. Brain. Res Bull 82: 201-207. doi:10.1016/j.brainresbull.2010.04.003.
52. Dogan I, Eickhoff SB, Schulz JB, Shah NJ, Laird AR, et al. (2012) Consistent Neurodegeneration and Its Association with Clinical Progression in Huntington's Disease: A Coordinate-Based Meta-Analysis. Neurodegener Dis, 12: 23-35. PubMed: 22922585.
53. Rosas HD, Koroshetz WJ, Chen YI, Skeuse C, Vangel M, et al. (2003) Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology 60: 1615-1620. doi:10.1212/01.WNL.0000065888.88988.6E. PubMed: 12771251.
54. Kassubek J, Gaus W, Landwehrmeyer GB, (2004) Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology 62: 523-524; author reply 524 doi:10.1212/WNL.62.3.523. PubMed: 14872054.
55. Lanska DJ, Lanska MJ, Lavine L, Schoenberg BS, (1988) Conditions associated with Huntington's disease at death. A case-control study. Arch Neurol 45: 878-880. doi:10.1001/archneur.1988.00520320068017. PubMed: 2969233.
56. Pattison JS, Sanbe A, Maloyan A, Osinska H, Klevitsky R, et al. (2008) Cardiomyocyte expression of a polyglutamine preamyloid oligomer causes heart failure. Circulation 117: 2743-2751. doi:10.1161/CIRCULATIONAHA.107.750232. PubMed: 18490523.
57. Mihm MJ, Amann DM, Schanbacher BL, Altschuld RA, Bauer JA, et al. (2007) Cardiac dysfunction in the R6/2 mouse model of Huntington's disease. Neurobiol Dis 25: 297-308. doi:10.1016/j.nbd.2006.09.016. PubMed: 17126554.
58. Andreassen OA, Dedeoglu A, Stanojevic V, Hughes DB, Browne SE, et al. (2002) Huntington's disease of the endocrine pancreas: insulin deficiency and diabetes mellitus due to impaired insulin gene expression. Neurobiol Dis 11: 410-424. doi:10.1006/nbdi.2002.0562. PubMed: 12586550.
59. Josefsen K, Nielsen MD, Jørgensen KH, Bock T, Nørremølle A, et al. (2008) Impaired glucose tolerance in the R6/1 transgenic mouse model of Huntington's disease. J Neuroendocrinol 20: 165-172. PubMed: 18034868.
60. Farrer LA, (1985) Diabetes mellitus in Huntington disease. Clin Genet 27: 62-67. PubMed: 3156696.
61. Consortium HDi (2012) Induced pluripotent stem cells from patients with Huntington's disease show CAG-repeat-expansion-associated phenotypes. Cell Stem Cell 11: 264-278. doi:10.1016/j.stem.2012.04.027. PubMed: 22748968.
62. Juopperi TA, Kim WR, Chiang CH, Yu H, Margolis RL, et al. (2012) Astrocytes generated from patient induced pluripotent stem cells recapitulate features of Huntington's disease patient cells. Mol Brain 5: 17. doi:10.1186/1756-6606-5-17. PubMed: 22613578.
63. Castiglioni V, Onorati M, Rochon C, Cattaneo E, (2012) Induced pluripotent stem cell lines from Huntington's disease mice undergo neuronal differentiation while showing alterations in the lysosomal pathway. Neurobiol Dis 46: 30-40. doi:10.1016/j.nbd.2011.12.032. PubMed: 22227000.
64. Jeon I, Lee N, Li JY, Park IH, Park KS, et al. (2012) Neuronal properties, in vivo effects, and pathology of a Huntington's disease patient-derived induced pluripotent stem cells. Stem Cells 30: 2054-2062. doi:10.1002/stem.1135. PubMed: 22628015.
65. Camnasio S, Delli Carri A, Lombardo A, Grad I, Mariotti C, et al. (2012) The first reported generation of several induced pluripotent stem cell lines from homozygous and heterozygous Huntington's disease patients demonstrates mutation related enhanced lysosomal activity. Neurobiol Dis 46: 41-51. doi:10.1016/j.nbd.2011.12.042. PubMed: 22405424.
66. Zhang N, An MC, Montoro D, Ellerby LM, (2010) Characterization of Human Huntington's Disease Cell Model from Induced Pluripotent Stem Cells. PLOS Curr 2RRN1193: RRN1193 PubMed: 21037797.
67. An MC, Zhang N, Scott G, Montoro D, Wittkop T, et al. (2012) Genetic correction of Huntington's disease phenotypes in induced pluripotent stem cells. Cell Stem Cell 11: 253-263. doi:10.1016/j.stem.2012.04.026. PubMed: 22748967.
68. Gao A, Peng Y, Deng Y, Qing H, (2013) Potential therapeutic applications of differentiated induced pluripotent stem cells (iPSCs) in the treatment of neurodegenerative diseases. Neuroscience 228: 47-59. doi:10.1016/j.neuroscience.2012.09.076. PubMed: 23069758.
69. Gunaseeli I, Doss MX, Antzelevitch C, Hescheler J, Sachinidis A, (2010) Induced pluripotent stem cells as a model for accelerated patient- and disease-specific drug discovery. Curr Med Chem 17: 759-766. doi:10.2174/092986710790514480. PubMed: 20088756.
70. Sohn YD, Han JW, Yoon YS, (2012) Generation of induced pluripotent stem cells from somatic cells. Prog Mol Biol. Transl Sci 111: 1-26.
71. Park IH, Arora N, Huo H, Maherali N, Ahfeldt T, et al. (2008) Disease-specific induced pluripotent stem cells. Cell 134: 877-886. doi:10.1016/j.cell.2008.07.041. PubMed: 18691744.
72. Marder K, Mehler MF, (2012) Development and neurodegeneration: turning HD pathogenesis on its head. Neurology 79: 621-622. doi:10.1212/WNL.0b013e3182648bfe. PubMed: 22815547.
73. Kurosawa H, (2007) Methods for inducing embryoid body formation: in vitro differentiation system of embryonic stem cells. J Biosci Bioeng 103: 389-398. doi:10.1263/jbb.103.389. PubMed: 17609152.
74. Okabe S, Forsberg-Nilsson K, Spiro AC, Segal M, McKay RD, (1996) Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech Dev 59: 89-102. doi:10.1016/0925-4773(96)00572-2. PubMed: 8892235.
75. Abrajano JJ, Qureshi IA, Gokhan S, Zheng D, Bergman A, et al. (2009) Differential deployment of REST and CoREST promotes glial subtype specification and oligodendrocyte lineage maturation. PLOS ONE 4: e7665. doi:10.1371/journal.pone.0007665. PubMed: 19888342.
76. Abrajano JJ, Qureshi IA, Gokhan S, Zheng D, Bergman A, et al. (2009) REST and CoREST modulate neuronal subtype specification, maturation and maintenance. PLOS ONE 4: e7936. doi:10.1371/journal.pone.0007936. PubMed: 19997604.
77. Yung SY, Gokhan S, Jurcsak J, Molero AE, Abrajano JJ, et al. (2002) Differential modulation of BMP signaling promotes the elaboration of cerebral cortical GABAergic neurons or oligodendrocytes from a common sonic hedgehog-responsive ventral forebrain progenitor species. Proc Natl Acad Sci U S A 99: 16273-16278. doi:10.1073/pnas.232586699. PubMed: 12461181.
78. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. doi:10.1006/meth.2001.1262. PubMed: 11846609.
79. Pfaffl MW, Horgan GW, Dempfle L, (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36. doi:10.1093/nar/30.9.e36. PubMed: 11972351.
80. Sun N, Lee A, Wu JC, (2009) Long term non-invasive imaging of embryonic stem cells using reporter genes. Nat Protoc 4: 1192-1201. doi:10.1038/nprot.2009.100. PubMed: 19617890.