A Rare Human Syndrome Provides Genetic Evidence that WNT Signaling Is Required for Reprogramming of Fibroblasts to Induced Pluripotent Stem Cells

Cell Reports

Volumn 9, Issue 5, 2014, Pages 1770-1780

  Ross, Jason ^a   Busch, Julia ^a   Mintz, Ellen ^b   Ng, Damian ^a   Stanley, Alexandra ^a   Brafman, David ^a   Sutton, V Reid ^c   Van den Veyver, Ignatia ^c,d   Willert, Karl ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CALIFORNIA POLYTECHNIC STATE UNIVERSITY   (United States)

^c TEXAS CHILDREN S HOSPITAL   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

WNT3A PROTEIN; BIOLOGICAL MARKER; TRANSCRIPTION FACTOR;

ARTICLE; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CONTROLLED STUDY; FIBROBLAST; GENE; GENE MUTATION; GENE OVEREXPRESSION; GOLTZ SYNDROME; HUMAN; HUMAN CELL; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PORCN GENE; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY; CELL CULTURE; CELL SHAPE; CELL TRANSDIFFERENTIATION; GENETIC TRANSDUCTION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

BIOMARKERS; CELL SHAPE; CELL TRANSDIFFERENTIATION; CELLS, CULTURED; CELLULAR REPROGRAMMING; FIBROBLASTS; FOCAL DERMAL HYPOPLASIA; HUMANS; INDUCED PLURIPOTENT STEM CELLS; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC; WNT SIGNALING PATHWAY;

EID: 84915820472     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.10.049     Document Type: Article

References (67)

1. Aoki K., Aoki M., Sugai M., Harada N., Miyoshi H., Tsukamoto T., Mizoshita T., Tatematsu M., Seno H., Chiba T., et al. Chromosomal instability by beta-catenin/TCF transcription in APC or beta-catenin mutant cells. Oncogene 2007, 26:3511-3520.
2. Aulicino F., Theka I., Ombrato L., Lluis F., Cosma M.P. Temporal perturbation of the Wnt signaling pathway in the control of cell reprogramming is modulated by TCF1. Stem Cell Rev. 2014, 2:707-720.
3. Bakre M.M., Hoi A., Mong J.C., Koh Y.Y., Wong K.Y., Stanton L.W. Generation of multipotential mesendodermal progenitors from mouse embryonic stem cells via sustained Wnt pathway activation. J.Biol. Chem. 2007, 282:31703-31712.
4. Barrott J.J., Cash G.M., Smith A.P., Barrow J.R., Murtaugh L.C. Deletion of mouse Porcn blocks Wnt ligand secretion and reveals an ectodermal etiology of human focal dermal hypoplasia/Goltz syndrome. Proc. Natl. Acad. Sci. USA 2011, 108:12752-12757.
5. Biechele S., Cox B.J., Rossant J. Porcupine homolog is required for canonical Wnt signaling and gastrulation in mouse embryos. Dev. Biol. 2011, 355:275-285.
6. Blauwkamp T.A., Nigam S., Ardehali R., Weissman I.L., Nusse R. Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. Nat Commun 2012, 3:1070.
7. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., Guenther M.G., Kumar R.M., Murray H.L., Jenner R.G., et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956.
8. Brafman D.A., Phung C., Kumar N., Willert K. Regulation of endodermal differentiation of human embryonic stem cells through integrin-ECM interactions. Cell Death Differ. 2013, 20:369-381.
9. Carmon K.S., Gong X., Lin Q., Thomas A., Liu Q. R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/beta-catenin signaling. Proc. Natl. Acad. Sci. USA 2011, 108:11452-11457.
10. Chen Y., Whetstone H.C., Lin A.C., Nadesan P., Wei Q., Poon R., Alman B.A. Beta-catenin signaling plays a disparate role in different phases of fracture repair: implications for therapy to improve bone healing. PLoS Med. 2007, 4:e249.
11. Chen B., Dodge M.E., Tang W., Lu J., Ma Z., Fan C.W., Wei S., Hao W., Kilgore J., Williams N.S., et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat. Chem. Biol. 2009, 5:100-107.
12. Chen G., Gulbranson D.R., Hou Z., Bolin J.M., Ruotti V., Probasco M.D., Smuga-Otto K., Howden S.E., Diol N.R., Propson N.E., et al. Chemically defined conditions for human iPSC derivation and culture. Nat. Methods 2011, 8:424-429.
13. Chua A.W., Ma D., Gan S.U., Fu Z., Han H.C., Song C., Sabapathy K., Phan T.T. The role of R-spondin2 in keratinocyte proliferation and epidermal thickening in keloid scarring. J.Invest. Dermatol. 2011, 131:644-654.
14. Cole M.F., Johnstone S.E., Newman J.J., Kagey M.H., Young R.A. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev. 2008, 22:746-755.
15. D'Amour K.A., Agulnick A.D., Eliazer S., Kelly O.G., Kroon E., Baetge E.E. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol. 2005, 23:1534-1541.
16. Davidson K.C., Adams A.M., Goodson J.M., McDonald C.E., Potter J.C., Berndt J.D., Biechele T.L., Taylor R.J., Moon R.T. Wnt/β-catenin signaling promotes differentiation, not self-renewal, of human embryonic stem cells and is repressed by Oct4. Proc. Natl. Acad. Sci. USA 2012, 109:4485-4490.
17. de Lau W., Barker N., Low T.Y., Koo B.K., Li V.S., Teunissen H., Kujala P., Haegebarth A., Peters P.J., van de Wetering M., et al. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature 2011, 476:293-297.
18. Dhamdhere G.R., Fang M.Y., Jiang J., Lee K., Cheng D., Olveda R.C., Liu B., Mulligan K.A., Carlson J.C., Ransom R.C., et al. Drugging a stem cell compartment using Wnt3a protein as a therapeutic. PLoS ONE 2014, 9:e83650.
19. Fathke C., Wilson L., Shah K., Kim B., Hocking A., Moon R., Isik F. Wnt signaling induces epithelial differentiation during cutaneous wound healing. BMC Cell Biol. 2006, 7:4.
20. Fernandez A., Huggins I.J., Perna L., Brafman D., Lu D., Yao S., Gaasterland T., Carson D.A., Willert K. The WNT receptor FZD7 is required for maintenance of the pluripotent state in human embryonic stem cells. Proc. Natl. Acad. Sci. USA 2014, 111:1409-1414.
21. Fodde R., Smits R., Clevers H. APC, signal transduction and genetic instability in colorectal cancer. Nat. Rev. Cancer 2001, 1:55-67.
22. Galli L.M., Barnes T.L., Secrest S.S., Kadowaki T., Burrus L.W. Porcupine-mediated lipid-modification regulates the activity and distribution of Wnt proteins in the chick neural tube. Development 2007, 134:3339-3348.
23. Green J.L., Bauer M., Yum K.W., Li Y.C., Cox M.L., Willert K., Wahl G.M. Use of a molecular genetic platform technology to produce human Wnt proteins reveals distinct local and distal signaling abilities. PLoS ONE 2013, 8:e58395.
24. Grzeschik K.H., Bornholdt D., Oeffner F., König A., del Carmen Boente M., Enders H., Fritz B., Hertl M., Grasshoff U., Höfling K., et al. Deficiency of PORCN, a regulator of Wnt signaling, is associated with focal dermal hypoplasia. Nat. Genet. 2007, 39:833-835.
25. Habib S.J., Chen B.C., Tsai F.C., Anastassiadis K., Meyer T., Betzig E., Nusse R. A localized Wnt signal orients asymmetric stem cell division invitro. Science 2013, 339:1445-1448.
26. Hadjihannas M.V., Behrens J. CIN By WNT: growth pathways, mitotic control and chromosomal instability in cancer. Cell Cycle 2006, 5:2077-2081.
27. Hadjihannas M.V., Brückner M., Jerchow B., Birchmeier W., Dietmaier W., Behrens J. Aberrant Wnt/beta-catenin signaling can induce chromosomal instability in colon cancer. Proc. Natl. Acad. Sci. USA 2006, 103:10747-10752.
28. Hao H.X., Xie Y., Zhang Y., Charlat O., Oster E., Avello M., Lei H., Mickanin C., Liu D., Ruffner H., et al. ZNRF3 promotes Wnt receptor turnover in an R-spondin-sensitive manner. Nature 2012, 485:195-200.
29. He T.C., Sparks A.B., Rago C., Hermeking H., Zawel L., da Costa L.T., Morin P.J., Vogelstein B., Kinzler K.W. Identification of c-MYC as a target of the APC pathway. Science 1998, 281:1509-1512.
30. Herr P., Basler K. Porcupine-mediated lipidation is required for Wnt recognition by Wls. Dev. Biol. 2012, 361:392-402.
31. Ho R., Papp B., Hoffman J.A., Merrill B.J., Plath K. Stage-specific regulation of reprogramming to induced pluripotent stem cells by Wnt signaling and Tcell factor proteins. Cell Rep 2013, 3:2113-2126.
32. Ishitani T., Kishida S., Hyodo-Miura J., Ueno N., Yasuda J., Waterman M., Shibuya H., Moon R.T., Ninomiya-Tsuji J., Matsumoto K. The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca(2+) pathway to antagonize Wnt/beta-catenin signaling. Mol. Cell. Biol. 2003, 23:131-139.
33. Janda C.Y., Waghray D., Levin A.M., Thomas C., Garcia K.C. Structural basis of Wnt recognition by Frizzled. Science 2012, 337:59-64.
34. Jiang W., Zhang D., Bursac N., Zhang Y. WNT3 is a biomarker capable of predicting the definitive endoderm differentiation potential of hESCs. Stem Cell Rev. 2013, 1:46-52.
35. Kadowaki T., Wilder E., Klingensmith J., Zachary K., Perrimon N. The segment polarity gene porcupine encodes a putative multitransmembrane protein involved in Wingless processing. Genes Dev. 1996, 10:3116-3128.
36. Kaplan K.B., Burds A.A., Swedlow J.R., Bekir S.S., Sorger P.K., Näthke I.S. A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat. Cell Biol. 2001, 3:429-432.
37. Kawakami Y., Rodriguez Esteban C., Raya M., Kawakami H., Martí M., Dubova I., Izpisúa Belmonte J.C. Wnt/beta-catenin signaling regulates vertebrate limb regeneration. Genes Dev. 2006, 20:3232-3237.
38. Kroon E., Martinson L.A., Kadoya K., Bang A.G., Kelly O.G., Eliazer S., Young H., Richardson M., Smart N.G., Cunningham J., et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells invivo. Nat. Biotechnol. 2008, 26:443-452.
39. Li W., Zhou H., Abujarour R., Zhu S., Young Joo J., Lin T., Hao E., Schöler H.R., Hayek A., Ding S. Generation of human-induced pluripotent stem cells in the absence of exogenous Sox2. Stem Cells 2009, 27:2992-3000.
40. Li Y., Zhang Q., Yin X., Yang W., Du Y., Hou P., Ge J., Liu C., Zhang W., Zhang X., et al. Generation of iPSCs from mouse fibroblasts with a single gene, Oct4, and small molecules. Cell Res. 2011, 21:196-204.
41. Lim X., Tan S.H., Koh W.L., Chau R.M., Yan K.S., Kuo C.J., van Amerongen R., Klein A.M., Nusse R. Interfollicular epidermal stem cells self-renew via autocrine Wnt signaling. Science 2013, 342:1226-1230.
42. Liu P., Wakamiya M., Shea M.J., Albrecht U., Behringer R.R., Bradley A. Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 1999, 22:361-365.
43. Liu W., Shaver T.M., Balasa A., Ljungberg M.C., Wang X., Wen S., Nguyen H., Van den Veyver I.B. Deletion of Porcn in mice leads to multiple developmental defects and models human focal dermal hypoplasia (Goltz syndrome). PLoS ONE 2012, 7:e32331.
44. Lyashenko N., Winter M., Migliorini D., Biechele T., Moon R.T., Hartmann C. Differential requirement for the dual functions of β-catenin in embryonic stem cell self-renewal and germ layer formation. Nat. Cell Biol. 2011, 13:753-761.
45. Marson A., Foreman R., Chevalier B., Bilodeau S., Kahn M., Young R.A., Jaenisch R. Wnt signaling promotes reprogramming of somatic cells to pluripotency. Cell Stem Cell 2008, 3:132-135.
46. Melchior K., Weiss J., Zaehres H., Kim Y.M., Lutzko C., Roosta N., Hescheler J., Müschen M. The WNT receptor FZD7 contributes to self-renewal signaling of human embryonic stem cells. Biol. Chem. 2008, 389:897-903.
47. Mikels A.J., Nusse R. Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol. 2006, 4:e115.
48. Proffitt K.D., Virshup D.M. Precise regulation of porcupine activity is required for physiological Wnt signaling. J.Biol. Chem. 2012, 287:34167-34178.
49. Ruffner H., Sprunger J., Charlat O., Leighton-Davies J., Grosshans B., Salathe A., Zietzling S., Beck V., Therier M., Isken A., et al. R-Spondin potentiates Wnt/β-catenin signaling through orphan receptors LGR4 and LGR5. PLoS ONE 2012, 7:e40976.
50. Sato N., Meijer L., Skaltsounis L., Greengard P., Brivanlou A.H. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 2004, 10:55-63.
51. Schulz T.C., Young H.Y., Agulnick A.D., Babin M.J., Baetge E.E., Bang A.G., Bhoumik A., Cepa I., Cesario R.M., Haakmeester C., et al. A scalable system for production of functional pancreatic progenitors from human embryonic stem cells. PLoS ONE 2012, 7:e37004.
52. Silva J., Barrandon O., Nichols J., Kawaguchi J., Theunissen T.W., Smith A. Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol. 2008, 6:e253.
53. Stoick-Cooper C.L., Weidinger G., Riehle K.J., Hubbert C., Major M.B., Fausto N., Moon R.T. Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 2007, 134:479-489.
54. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
55. Temple I.K., MacDowall P., Baraitser M., Atherton D.J. Focal dermal hypoplasia (Goltz syndrome). J.Med. Genet. 1990, 27:180-187.
56. ten Berge D., Kurek D., Blauwkamp T., Koole W., Maas A., Eroglu E., Siu R.K., Nusse R. Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nat. Cell Biol. 2011, 13:1070-1075.
57. Tighe A., Ray-Sinha A., Staples O.D., Taylor S.S. GSK-3 inhibitors induce chromosome instability. BMC Cell Biol. 2007, 8:34.
58. van den Heuvel M., Harryman-Samos C., Klingensmith J., Perrimon N., Nusse R. Mutations in the segment polarity genes wingless and porcupine impair secretion of the wingless protein. EMBO J. 1993, 12:5293-5302.
59. Wang X., Reid Sutton V., Omar Peraza-Llanes J., Yu Z., Rosetta R., Kou Y.C., Eble T.N., Patel A., Thaller C., Fang P., Van den Veyver I.B. Mutations in X-linked PORCN, a putative regulator of Wnt signaling, cause focal dermal hypoplasia. Nat. Genet. 2007, 39:836-838.
60. Wei Q., Yokota C., Semenov M.V., Doble B., Woodgett J., He X. R-spondin1 is a high affinity ligand for LRP6 and induces LRP6 phosphorylation and beta-catenin signaling. J.Biol. Chem. 2007, 282:15903-15911.
61. Whyte J.L., Smith A.A., Liu B., Manzano W.R., Evans N.D., Dhamdhere G.R., Fang M.Y., Chang H.Y., Oro A.E., Helms J.A. Augmenting endogenous Wnt signaling improves skin wound healing. PLoS ONE 2013, 8:e76883.
62. Willert K.H. Isolation and application of bioactive Wnt proteins. Methods Mol. Biol. 2008, 468:17-29.
63. Wray J., Kalkan T., Gomez-Lopez S., Eckardt D., Cook A., Kemler R., Smith A. Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Nat. Cell Biol. 2011, 13:838-845.
64. Yi F., Pereira L., Hoffman J.A., Shy B.R., Yuen C.M., Liu D.R., Merrill B.J. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat. Cell Biol. 2011, 13:762-770.
65. Zhai L., Chaturvedi D., Cumberledge S. Drosophila wnt-1 undergoes a hydrophobic modification and is targeted to lipid rafts, a process that requires porcupine. J.Biol. Chem. 2004, 279:33220-33227.
66. Zhang S., Li Y., Wu Y., Shi K., Bing L., Hao J. Wnt/β-catenin signaling pathway upregulates c-Myc expression to promote cell proliferation of P19 teratocarcinoma cells. Anat. Rec. (Hoboken) 2012, 295:2104-2113.
67. Zhang P., Chang W.H., Fong B., Gao F., Liu C., Al Alam D., Bellusci S., Lu W. Regulation of iPS cell induction by Wnt/beta-catenin signaling. J.Biol. Chem. 2014, 289:9221-9232.