Gata6-Dependent GLI3 Repressor Function is Essential in Anterior Limb Progenitor Cells for Proper Limb Development

PLoS Genetics

Volumn 12, Issue 6, 2016, Pages

  Hayashi, Shinichi ^a,b   Akiyama, Ryutaro ^a,b   Wong, Julia ^a   Tahara, Naoyuki ^a,b   Kawakami, Hiroko ^a,b   Kawakami, Yasuhiko ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR GLI3; GATA6 PROTEIN, HUMAN; GLI3 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; NERVE PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL ANALYSIS; CONTROLLED STUDY; EMBRYO; GATA6 GENE; GENE EXPRESSION; GENE INACTIVATION; GENE INTERACTION; GENE MUTATION; GENE REPRESSION; GENETIC ANALYSIS; GLI3 GENE; HETEROZYGOTE; HINDLIMB; HUMAN; HUMAN CELL; IN VITRO STUDY; LIMB BUD; LIMB DEVELOPMENT; LIMB MALFORMATION; NONHUMAN; POLYDACTYLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SHH GENE; STEM CELL; TRANSCRIPTION REGULATION; 3T3 CELL LINE; ANIMAL; CELL LINE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEK293 CELL LINE; LIMB; METABOLISM; MORPHOGENESIS; MOUSE; ORGANOGENESIS; SIGNAL TRANSDUCTION;

ANIMALS; BODY PATTERNING; CELL LINE; EXTREMITIES; GATA6 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HEK293 CELLS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LIMB BUDS; MICE; NERVE TISSUE PROTEINS; NIH 3T3 CELLS; ORGANOGENESIS; POLYDACTYLY; SIGNAL TRANSDUCTION; STEM CELLS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84977566610     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006138     Document Type: Article

References (73)

1. Zeller R, Lopez-Rios J, Zuniga A, Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet. 2009;10(12):845–58. 19920852. doi: 10.1038/nrg2681
2. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, et al. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature. 1996;383(6599):407–13. 8837770.
3. Riddle RD, Johnson RL, Laufer E, Tabin C, Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 1993;75(7):1401–16. 8269518.
4. Yang Y, Drossopoulou G, Chuang PT, Duprez D, Marti E, Bumcrot D, et al. Relationship between dose, distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development (Cambridge, England). 1997;124(21):4393–404. 9334287.
5. Harfe BD, Scherz PJ, Nissim S, Tian H, McMahon AP, Tabin CJ, Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell. 2004;118(4):517–28. 15315763.
6. Ahn S, Joyner AL, Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell. 2004;118(4):505–16. 15315762.
7. Towers M, Mahood R, Yin Y, Tickle C, Integration of growth and specification in chick wing digit-patterning. Nature. 2008;452(7189):882–6. 18354396. doi: 10.1038/nature06718
8. Zhu J, Nakamura E, Nguyen MT, Bao X, Akiyama H, Mackem S, Uncoupling Sonic hedgehog control of pattern and expansion of the developing limb bud. Developmental cell. 2008;14(4):624–32. 18410737. doi: 10.1016/j.devcel.2008.01.008
9. Masuya H, Sagai T, Wakana S, Moriwaki K, Shiroishi T, A duplicated zone of polarizing activity in polydactylous mouse mutants. Genes & development. 1995;9(13):1645–53. Epub 1995/07/01. 7628698.
10. Chiang C, Litingtung Y, Harris MP, Simandl BK, Li Y, Beachy PA, et al. Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Developmental biology. 2001;236(2):421–35. 11476582.
11. Kraus P, Fraidenraich D, Loomis CA, Some distal limb structures develop in mice lacking Sonic hedgehog signaling. Mechanisms of development. 2001;100(1):45–58. 11118883.
12. Li D, Sakuma R, Vakili NA, Mo R, Puviindran V, Deimling S, et al. Formation of proximal and anterior limb skeleton requires early function of Irx3 and Irx5 and is negatively regulated by Shh signaling. Developmental cell. 2014;29(2):233–40. 24726282. doi: 10.1016/j.devcel.2014.03.001
13. Akiyama R, Kawakami H, Wong J, Oishi I, Nishinakamura R, Kawakami Y, Sall4-Gli3 system in early limb progenitors is essential for the development of limb skeletal elements. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(16):5075–80. doi: 10.1073/pnas.142194911225848055; PubMed Central PMCID: PMCPMC4413345.
14. Hui CC, Angers S, Gli proteins in development and disease. Annu Rev Cell Dev Biol. 2011;27:513–37. Epub 2011/08/02. doi: 10.1146/annurev-cellbio-092910-15404821801010.
15. Wen X, Lai CK, Evangelista M, Hongo JA, de Sauvage FJ, Scales SJ, Kinetics of hedgehog-dependent full-length Gli3 accumulation in primary cilia and subsequent degradation. Molecular and cellular biology. 2010;30(8):1910–22. doi: 10.1128/MCB.01089-0920154143; PubMed Central PMCID: PMCPMC2849461.
16. McDermott A, Gustafsson M, Elsam T, Hui CC, Emerson CP, Jr.Borycki AG, Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation. Development (Cambridge, England). 2005;132(2):345–57. doi: 10.1242/dev.0153715604102.
17. Pan Y, Bai CB, Joyner AL, Wang B, Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Molecular and cellular biology. 2006;26(9):3365–77. doi: 10.1128/MCB.26.9.3365–3377.200616611981; PubMed Central PMCID: PMCPMC1447407.
18. Wang B, Fallon JF, Beachy PA, Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell. 2000;100(4):423–34. 10693759.
19. Winter RM, Huson SM, Greig cephalopolysyndactyly syndrome: a possible mouse homologue (Xt-extra toes). Am J Med Genet. 1988;31(4):793–8. doi: 10.1002/ajmg.13203104113239570.
20. Pettigrew AL, Greenberg F, Caskey CT, Ledbetter DH, Greig syndrome associated with an interstitial deletion of 7p: confirmation of the localization of Greig syndrome to 7p13. Hum Genet. 1991;87(4):452–6. 1879832.
21. Hui CC, Joyner AL, A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nature genetics. 1993;3(3):241–6. Epub 1993/03/01. doi: 10.1038/ng0393-2418387379.
22. Hu MC, Mo R, Bhella S, Wilson CW, Chuang PT, Hui CC, et al. GLI3-dependent transcriptional repression of Gli1, Gli2 and kidney patterning genes disrupts renal morphogenesis. Development (Cambridge, England). 2006;133(3):569–78. doi: 10.1242/dev.0222016396903.
23. Buscher D, Bosse B, Heymer J, Ruther U, Evidence for genetic control of Sonic hedgehog by Gli3 in mouse limb development. Mechanisms of development. 1997;62(2):175–82. Epub 1997/03/01. S0925-4773(97)00656-4 [pii]. 9152009.
24. Wang C, Ruther U, Wang B, The Shh-independent activator function of the full-length Gli3 protein and its role in vertebrate limb digit patterning. Developmental biology. 2007;305(2):460–9. 17400206.
25. te Welscher P, Zuniga A, Kuijper S, Drenth T, Goedemans HJ, Meijlink F, et al. Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science New York, NY. 2002;298(5594):827–30. 12215652.
26. Litingtung Y, Dahn RD, Li Y, Fallon JF, Chiang C, Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature. 2002;418(6901):979–83. 12198547.
27. Aberger F, Ruiz IAA, Context-dependent signal integration by the GLI code: the oncogenic load, pathways, modifiers and implications for cancer therapy. Seminars in cell & developmental biology. 2014;33:93–104. doi: 10.1016/j.semcdb.2014.05.00324852887; PubMed Central PMCID: PMCPMC4151135.
28. Briscoe J, Therond PP, The mechanisms of Hedgehog signalling and its roles in development and disease. Nature reviews. 2013;14(7):416–29. doi: 10.1038/nrm359823719536.
29. Sheth R, Bastida MF, Ros M, Hoxd and Gli3 interactions modulate digit number in the amniote limb. Developmental biology. 2007;310(2):430–41. doi: 10.1016/j.ydbio.2007.07.02317714700.
30. Panman L, Drenth T, Tewelscher P, Zuniga A, Zeller R, Genetic interaction of Gli3 and Alx4 during limb development. The International journal of developmental biology. 2005;49(4):443–8. Epub 2005/06/22. 051984lp [pii] doi: 10.1387/ijdb.051984lp15968591.
31. Quinn ME, Haaning A, Ware SM, Preaxial polydactyly caused by Gli3 haploinsufficiency is rescued by Zic3 loss of function in mice. Human molecular genetics. 2012;21(8):1888–96. Epub 2012/01/12. doi: 10.1093/hmg/dds002 [pii]. 22234993; PubMed Central PMCID: PMC3313802.
32. Chlon TM, Crispino JD, Combinatorial regulation of tissue specification by GATA and FOG factors. Development (Cambridge, England). 2012;139(21):3905–16. doi: 10.1242/dev.08044023048181; PubMed Central PMCID: PMCPMC3472596.
33. Molkentin JD, The zinc finger-containing transcription factors GATA-4, -5, and -6. Ubiquitously expressed regulators of tissue-specific gene expression. The Journal of biological chemistry. 2000;275(50):38949–52. doi: 10.1074/jbc.R00002920011042222.
34. Morrisey EE, Tang Z, Sigrist K, Lu MM, Jiang F, Ip HS, et al. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes & development. 1998;12(22):3579–90. 9832509; PubMed Central PMCID: PMCPMC317242.
35. Koutsourakis M, Langeveld A, Patient R, Beddington R, Grosveld F, The transcription factor GATA6 is essential for early extraembryonic development. Development (Cambridge, England). 1999;126(9):723–32. 10383242.
36. Zhao R, Watt AJ, Battle MA, Li J, Bondow BJ, Duncan SA, Loss of both GATA4 and GATA6 blocks cardiac myocyte differentiation and results in acardia in mice. Developmental biology. 2008;317(2):614–9. doi: 10.1016/j.ydbio.2008.03.01318400219; PubMed Central PMCID: PMCPMC2423416.
37. Decker K, Goldman DC, Grasch CL, Sussel L, Gata6 is an important regulator of mouse pancreas development. Developmental biology. 2006;298(2):415–29. doi: 10.1016/j.ydbio.2006.06.04616887115; PubMed Central PMCID: PMCPMC2824170.
38. Kozhemyakina E, Ionescu A, Lassar AB, GATA6 is a crucial regulator of Shh in the limb bud. PLoS Genet. 2014;10(1):e1004072. Epub 2014/01/15. doi: 10.1371/journal.pgen.1004072 PGENETICS-D-13-01628 [pii]. 24415953; PubMed Central PMCID: PMC3886911.
39. Karamboulas K, Dranse HJ, Underhill TM, Regulation of BMP-dependent chondrogenesis in early limb mesenchyme by TGFbeta signals. Journal of cell science. 2010;123(Pt 12):2068–76. Epub 2010/05/27. doi: 10.1242/jcs.062901 [pii]. 20501701.
40. Alexandrovich A, Qureishi A, Coudert AE, Zhang L, Grigoriadis AE, Shah AM, et al. A role for GATA-6 in vertebrate chondrogenesis. Developmental biology. 2008;314(2):457–70. Epub 2008/01/15. doi: 10.1016/j.ydbio.2007.12.001 S0012-1606(07)01570-9 [pii]. 18191120.
41. Sodhi CP, Li J, Duncan SA, Generation of mice harbouring a conditional loss-of-function allele of Gata6. BMC developmental biology. 2006;6:19. 16611361.
42. Perantoni AO, Timofeeva O, Naillat F, Richman C, Pajni-Underwood S, Wilson C, et al. Inactivation of FGF8 in early mesoderm reveals an essential role in kidney development. Development (Cambridge, England). 2005;132(17):3859–71. 16049111.
43. Xin M, Davis CA, Molkentin JD, Lien CL, Duncan SA, Richardson JA, et al. A threshold of GATA4 and GATA6 expression is required for cardiovascular development. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(30):11189–94. Epub 2006/07/19. 0604604103 [pii] doi: 10.1073/pnas.060460410316847256; PubMed Central PMCID: PMC1544063.
44. Galli A, Robay D, Osterwalder M, Bao X, Benazet JD, Tariq M, et al. Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. PLoS Genet. 2010;6(4):e1000901. Epub 2010/04/14. doi: 10.1371/journal.pgen.100090120386744; PubMed Central PMCID: PMC2851570.
45. Qu S, Tucker SC, Ehrlich JS, Levorse JM, Flaherty LA, Wisdom R, et al. Mutations in mouse Aristaless-like4 cause Strong's luxoid polydactyly. Development (Cambridge, England). 1998;125(14):2711–21. 9636085.
46. Zhang Z, Verheyden JM, Hassell JA, Sun X, FGF-regulated Etv genes are essential for repressing Shh expression in mouse limb buds. Developmental cell. 2009;16(4):607–13. Epub 2009/04/24. S1534-5807(09)00082-3 [pii] doi: 10.1016/j.devcel.2009.02.00819386269.
47. Mao J, McGlinn E, Huang P, Tabin CJ, McMahon AP, Fgf-dependent Etv4/5 activity is required for posterior restriction of Sonic Hedgehog and promoting outgrowth of the vertebrate limb. Developmental cell. 2009;16(4):600–6. Epub 2009/04/24. S1534-5807(09)00079-3 [pii] doi: 10.1016/j.devcel.2009.02.00519386268; PubMed Central PMCID: PMC3164484.
48. Bourgeois P, Bolcato-Bellemin AL, Danse JM, Bloch-Zupan A, Yoshiba K, Stoetzel C, et al. The variable expressivity and incomplete penetrance of the twist-null heterozygous mouse phenotype resemble those of human Saethre-Chotzen syndrome. Human molecular genetics. 1998;7(6):945–57. 9580658.
49. Zhang Z, Sui P, Dong A, Hassell J, Cserjesi P, Chen YT, et al. Preaxial polydactyly: interactions among ETV, TWIST1 and HAND2 control anterior-posterior patterning of the limb. Development (Cambridge, England). 2010;137(20):3417–26. Epub 2010/09/10. dev.051789 [pii] doi: 10.1242/dev.05178920826535; PubMed Central PMCID: PMC2947755.
50. Patterson VL, Damrau C, Paudyal A, Reeve B, Grimes DT, Stewart ME, et al. Mouse hitchhiker mutants have spina bifida, dorso-ventral patterning defects and polydactyly: identification of Tulp3 as a novel negative regulator of the Sonic hedgehog pathway. Human molecular genetics. 2009;18(10):1719–39. Epub 2009/02/19. ddp075 [pii] doi: 10.1093/hmg/ddp07519223390; PubMed Central PMCID: PMC2671985.
51. Norman RX, Ko HW, Huang V, Eun CM, Abler LL, Zhang Z, et al. Tubby-like protein 3 (TULP3) regulates patterning in the mouse embryo through inhibition of Hedgehog signaling. Human molecular genetics. 2009;18(10):1740–54. Epub 2009/03/17. ddp113 [pii] doi: 10.1093/hmg/ddp11319286674; PubMed Central PMCID: PMC2671991.
52. Cameron DA, Pennimpede T, Petkovich M, Tulp3 is a critical repressor of mouse hedgehog signaling. Dev Dyn. 2009;238(5):1140–9. Epub 2009/04/01. doi: 10.1002/dvdy.2192619334287.
53. Wright E, Hargrave MR, Christiansen J, Cooper L, Kun J, Evans T, et al. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nature genetics. 1995;9(1):15–20. 7704017.
54. Mo R, Freer AM, Zinyk DL, Crackower MA, Michaud J, Heng HH, et al. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development (Cambridge, England). 1997;124(1):113–23. Epub 1997/01/01. 9006072.
55. Lopez-Rios J, Speziale D, Robay D, Scotti M, Osterwalder M, Nusspaumer G, et al. GLI3 constrains digit number by controlling both progenitor proliferation and BMP-dependent exit to chondrogenesis. Developmental cell. 2012;22(4):837–48. Epub 2012/04/03. doi: 10.1016/j.devcel.2012.01.006 S1534-5807(12)00040-8 [pii]. 22465667.
56. McGlinn E, van Bueren KL, Fiorenza S, Mo R, Poh AM, Forrest A, et al. Pax9 and Jagged1 act downstream of Gli3 in vertebrate limb development. Mechanisms of development. 2005;122(11):1218–33. 16169709.
57. Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, et al. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes & development. 1998;12(20):3156–61. 9784490.
58. Dickinson RJ, Eblaghie MC, Keyse SM, Morriss-Kay GM, Expression of the ERK-specific MAP kinase phosphatase PYST1/MKP3 in mouse embryos during morphogenesis and early organogenesis. Mechanisms of development. 2002;113(2):193–6. 11960712
59. Klock A, Herrmann BG, Cloning and expression of the mouse dual-specificity mitogen-activated protein (MAP) kinase phosphatase Mkp3 during mouse embryogenesis. Mechanisms of development. 2002;116(1–2):243–7. 12128234
60. Kawakami Y, Rodriguez-Leon J, Koth CM, Buscher D, Itoh T, Raya A, et al. MKP3 mediates the cellular response to FGF8 signalling in the vertebrate limb. Nature cell biology. 2003;5(6):513–9. 12766772.
61. Qu S, Niswender KD, Ji Q, van der Meer R, Keeney D, Magnuson MA, et al. Polydactyly and ectopic ZPA formation in Alx-4 mutant mice. Development (Cambridge, England). 1997;124(20):3999–4008. Epub 1997/11/28. 9374397.
62. Lettice LA, Horikoshi T, Heaney SJ, van Baren MJ, van der Linde HC, Breedveld GJ, et al. Disruption of a long-range cis-acting regulator for Shh causes preaxial polydactyly. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(11):7548–53. 12032320.
63. Charite J, McFadden DG, Olson EN, The bHLH transcription factor dHAND controls Sonic hedgehog expression and establishment of the zone of polarizing activity during limb development. Development (Cambridge, England). 2000;127(11):2461–70. Epub 2000/05/11. 10804186.
64. Zakany J, Zacchetti G, Duboule D, Interactions between HOXD and Gli3 genes control the limb apical ectodermal ridge via Fgf10. Developmental biology. 2007;306(2):883–93. 17467687.
65. Hill P, Gotz K, Ruther U, A SHH-independent regulation of Gli3 is a significant determinant of anteroposterior patterning of the limb bud. Developmental biology. 2009;328(2):506–16. doi: 10.1016/j.ydbio.2009.02.01719248778.
66. Daoud G, Kempf H, Kumar D, Kozhemyakina E, Holowacz T, Kim DW, et al. BMP-mediated induction of GATA4/5/6 blocks somitic responsiveness to SHH. Development (Cambridge, England). 2014;141(20):3978–87. doi: 10.1242/dev.11190625294942; PubMed Central PMCID: PMCPMC4197703.
67. Nardelli J, Thiesson D, Fujiwara Y, Tsai FY, Orkin SH, Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Developmental biology. 1999;210(2):305–21. doi: 10.1006/dbio.1999.927810357893.
68. Ruest LB, Xiang X, Lim KC, Levi G, Clouthier DE, Endothelin-A receptor-dependent and -independent signaling pathways in establishing mandibular identity. Development (Cambridge, England). 2004;131(18):4413–23. doi: 10.1242/dev.0129115306564; PubMed Central PMCID: PMCPMC2818681.
69. Buscher D, Grotewold L, Ruther U, The XtJ allele generates a Gli3 fusion transcript. Mamm Genome. 1998;9(8):676–8. 9680393.
70. Kawakami Y, Tsuda M, Takahashi S, Taniguchi N, Esteban CR, Zemmyo M, et al. Transcriptional coactivator PGC-1alpha regulates chondrogenesis via association with Sox9. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(7):2414–9. 15699338.
71. Zhong Y, Wang Z, Fu B, Pan F, Yachida S, Dhara M, et al. GATA6 activates Wnt signaling in pancreatic cancer by negatively regulating the Wnt antagonist Dickkopf-1. PloS one. 2011;6(7):e22129. doi: 10.1371/journal.pone.002212921811562; PubMed Central PMCID: PMCPMC3139620.
72. Osterwalder M, Speziale D, Shoukry M, Mohan R, Ivanek R, Kohler M, et al. HAND2 targets define a network of transcriptional regulators that compartmentalize the early limb bud mesenchyme. Developmental cell. 2014;31(3):345–57. Epub 2014/12/03. doi: 10.1016/j.devcel.2014.09.018 S1534-5807(14)00624-8 [pii]. 25453830.
73. Suzuki A, Raya A, Kawakami Y, Morita M, Matsui T, Nakashima K, et al. Nanog binds to Smad1 and blocks bone morphogenetic protein-induced differentiation of embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(27):10294–9. 16801560.