Distinct cellular origin and genetic requirement of Hedgehog-Gli in postnatal rhabdomyosarcoma genesis

Oncogene

Volumn 33, Issue 46, 2014, Pages 5370-5378

  Rajurkar, M ^a   Huang, H ^a,b   Cotton, J L ^a   Brooks, J K ^a,e   Sicklick, J ^c   McMahon, A P ^d   Mao, J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b Central South University   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Gli; Hedgehog; progenitor; rhbdomyosarcoma

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GLI PROTEIN, MOUSE; GLI3 PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; NERVE PROTEIN; PAX7 PROTEIN, MOUSE; SMO PROTEIN, MOUSE; SONIC HEDGEHOG PROTEIN; SOX11 PROTEIN, MOUSE; SOX4 PROTEIN, MOUSE; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR PAX7; TRANSCRIPTION FACTOR SOX;

129 MOUSE; ANIMAL; CELL CULTURE; CELL LINEAGE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOBLOTTING; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHABDOMYOSARCOMA; RNA INTERFERENCE; SKELETAL MUSCLE SATELLITE CELL; TUMOR CELL CULTURE;

ANIMALS; CELL LINEAGE; CELLS, CULTURED; GENE EXPRESSION REGULATION, NEOPLASTIC; HEDGEHOG PROTEINS; HUMANS; IMMUNOBLOTTING; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE, 129 STRAIN; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PAX7 TRANSCRIPTION FACTOR; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHABDOMYOSARCOMA; RNA INTERFERENCE; SATELLITE CELLS, SKELETAL MUSCLE; SOXC TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

EID: 85027950593     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.480     Document Type: Article

References (65)

1. McMahon AP, Ingham PW, Tabin CJ. Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 2003; 53: 1–114. DOI: 10.1016/S0070-2153(03)53002-2
2. Jiang J, Hui CC. Hedgehog signaling in development and cancer. Dev Cell 2008; 15: 801–812. DOI: 10.1016/j.devcel.2008.11.010
3. Barakat MT, Humke EW, Scott MP. Learning from Jekyll to control Hyde: Hedgehog signaling in development and cancer. Trends Mol Med 2010; 16: 337–348. DOI: 10.1016/j.molmed.2010.05.003
4. Lum L, Beachy PA. The Hedgehog response network: sensors, switches, and routers. Science 2004; 304: 1755–1759. DOI: 10.1126/science.1098020
5. Hooper JE, Scott MP. Communicating with Hedgehogs. Nat Rev Mol Cell Biol 2005; 6: 306–317. DOI: 10.1038/nrm1622
6. Hui CC, Angers S. Gli Proteins in Development and Disease. Annu Rev Cell Dev Biol 2011; 27: 23.21–23.25. DOI: 10.1146/annurev-cellbio-092910-154048
7. Stecca B, Ruiz IAA. Context-dependent regulation of the GLI code in cancer by HEDGEHOG and non-HEDGEHOG signals. J Mol Cell Biol 2010; 2: 84–95. DOI: 10.1093/jmcb/mjp052
8. Gorlin RJ. Nevoid basal-cell carcinoma syndrome. Medicine (Baltimore) 1987; 66: 98–113. DOI: 10.1097/00005792-198703000-00002
9. Rubin LL, de Sauvage FJ. Targeting the Hedgehog pathway in cancer. Nat Rev Drug Discov 2006; 5: 1026–1033. DOI: 10.1038/nrd2086
10. Teglund S, Toftgard R. Hedgehog beyond medulloblastoma and basal cell carcinoma. Biochim Biophys Acta 2010; 1805: 181–208.
11. Johnson RL, Rothman AL, Xie J, Goodrich LV, Bare JW, Bonifas JM et al. Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 1996; 272: 1668–1671. DOI: 10.1126/science.272.5268.1668
12. Hahn H, Wicking C, Zaphiropoulous PG, Gailani MR, Shanley S, Chidambaram A et al. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 1996; 85: 841–851. DOI: 10.1016/S0092-8674(00)81268-4
13. Oro AE, Higgins KM, Hu Z, Bonifas JM, Epstein EH Jr., Scott MP. Basal cell carcinomas in mice overexpressing sonic hedgehog. Science 1996; 276: 817–821. DOI: 10.1126/science.276.5313.817
14. Xie J, Murone M, Luoh SM, Ryan A, Gu Q, Zhang C et al. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 1998; 391: 90–92. DOI: 10.1038/34201
15. Aszterbaum M, Epstein J, Oro A, Douglas V, LeBoit PE, Scott MP et al. Ultraviolet and ionizing radiation enhance the growth of BCCs and trichoblastomas in patched heterozygous knockout mice. Nat Med 1999; 5: 1285–1291. DOI: 10.1038/15242
16. Grachtchouk M, Mo R, Yu S, Zhang X, Sasaki H, Hui CC et al. Basal cell carcinomas in mice overexpressing Gli2 in skin. Nat Genet 2000; 24: 216–217. DOI: 10.1038/73417
17. Mao J, Ligon KL, Rakhlin EY, Thayer SP, Bronson RT, Rowitch D et al. A novel somatic mouse model to survey tumorigenic potential applied to the Hedgehog pathway. Cancer Res 2006; 66: 10171–10178. DOI: 10.1158/0008-5472.CAN-06-0657
18. Schuller U, Heine VM, Mao J, Kho AT, Dillon AK, Han YG et al. Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 2008; 14: 123–134. DOI: 10.1016/j.ccr.2008.07.005
19. Wechsler-Reya RJ, Scott MP. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 1999; 22: 103–114. DOI: 10.1016/S0896-6273(00)80682-0
20. Rowitch DH, S-Jacques B, Lee SM, Flax JD, Snyder EY, McMahon AP. Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells. J Neurosci 1999; 19: 8954–8965. DOI: 10.1523/JNEUROSCI.19-20-08954.1999
21. Oliver TG, Read TA, Kessler JD, Mehmeti A, Wells JF, Huynh TT et al. Loss of patched and disruption of granule cell development in a pre-neoplastic stage of medulloblastoma. Development 2005; 132: 2425–2439. DOI: 10.1242/dev.01793
22. Gibson P, Tong Y, Robinson G, Thompson MC, Currle DS, Eden C et al. Subtypes of medulloblastoma have distinct developmental origins. Nature 2010; 468: 1095–1099. DOI: 10.1038/nature09587
23. Youssef KK, Van Keymeulen A, Lapouge G, Beck B, Michaux C, Achouri Y et al. Identification of the cell lineage at the origin of basal cell carcinoma. Nat Cell Biol 2010; 12: 299–305. DOI: 10.1038/ncb2031
24. Ridky TW, Khavari PA. The hair follicle bulge stem cell niche resists transformation by the hedgehog pathway. Cell Stem Cell 2010; 6: 292–294. DOI: 10.1016/j.stem.2010.03.009
25. Grachtchouk M, Pero J, Yang SH, Ermilov AN, Michael LE, Wang A et al. Basal cell carcinomas in mice arise from hair follicle stem cells and multiple epithelial progenitor populations. J Clin Invest 2011; 121: 1768–1781. DOI: 10.1172/JCI46307
26. Wang GY, Wang J, Mancianti ML, Epstein EH Jr. Basal cell carcinomas arise from hair follicle stem cells in Ptch1(+/−) mice. Cancer Cell 2011; 19: 114–124. DOI: 10.1016/j.ccr.2010.11.007
27. Pappo AS. Rhabdomyosarcoma and other soft tissue sarcomas of childhood. Curr Opin Oncol 1995; 7: 361–366. DOI: 10.1097/00001622-199507000-00012
28. Merlino G, Helman LJ. Rhabdomyosarcoma—working out the pathways. Oncogene 1999; 18: 5340–5348. DOI: 10.1038/sj.onc.1203038
29. Breneman JC, Lyden E, Pappo AS, Link MP, Anderson JR, Parham DM et al. Prognostic factors and clinical outcomes in children and adolescents with metastatic rhabdomyosarcoma—a report from the Intergroup Rhabdomyosarcoma Study IV. J Clin Oncol 2003; 21: 78–84. DOI: 10.1200/JCO.2003.06.129
30. Hettmer S, Wagers AJ. Muscling in: uncovering the origins of rhabdomyosarcoma. Nat Med 2010; 16: 171–173. DOI: 10.1038/nm0210-171
31. Roberts WM, Douglass EC, Peiper SC, Houghton PJ, Look AT. Amplification of the gli gene in childhood sarcomas. Cancer Res 1989; 49: 5407–5413.
32. Bridge JA, Liu J, Weibolt V, Baker KS, Perry D, Kruger R et al. Novel genomic imbalances in embryonal rhabdomyosarcoma revealed by comparative genomic hybridization and fluorescence in situ hybridization: an intergroup rhabdomyosarcoma study. Genes Chromosomes Cancer 2000; 27: 337–344. DOI: 10.1002/(SICI)1098-2264(200004)27:4<337::AID-GCC1>3.0.CO;2-1
33. Bridge JA, Liu J, Qualman SJ, Suijkerbuijk R, Wenger G, Zhang J et al. Genomic gains and losses are similar in genetic and histologic subsets of rhabdomyosarcoma, whereas amplification predominates in embryonal with anaplasia and alveolar subtypes. Genes Chromosomes Cancer 2002; 33: 310–321. DOI: 10.1002/gcc.10026
34. Tostar U, Malm CJ, Meis-Kindblom JM, Kindblom LG, Toftgard R, Unden AB. Deregulation of the hedgehog signalling pathway: a possible role for the PTCH and SUFU genes in human rhabdomyoma and rhabdomyosarcoma development. J Pathol 2006; 208: 17–25. DOI: 10.1002/path.1882
35. Zibat A, Missiaglia E, Rosenberger A, Pritchard-Jones K, Shipley J, Hahn H et al. Activation of the hedgehog pathway confers a poor prognosis in embryonal and fusion gene-negative alveolar rhabdomyosarcoma. Oncogene 2010; 29: 6323–6330. DOI: 10.1038/onc.2010.368
36. Hayashi S, McMahon AP. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 2002; 244: 305–318. DOI: 10.1006/dbio.2002.0597
37. 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: 517–528. DOI: 10.1016/j.cell.2004.07.024
38. Ahn S, Joyner AL. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 2004; 118: 505–516. DOI: 10.1016/j.cell.2004.07.023
39. Lee J, Platt KA, Censullo P, Ruiz i Altaba A. Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 1997; 124: 2537–2552.
40. Bai CB, Auerbach W, Lee JS, Stephen D, Joyner AL. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 2002; 129: 4753–4761. DOI: 10.1242/dev.00115
41. Ahn S, Joyner AL. In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 2005; 437: 894–897. DOI: 10.1038/nature03994
42. Brownell I, Guevara E, Bai CB, Loomis CA, Joyner AL. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 2011; 8: 552–565. DOI: 10.1016/j.stem.2011.02.021
43. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999; 21: 70–71. DOI: 10.1038/5007
44. Tiffin N, Williams RD, Shipley J, Pritchard-Jones K. PAX7 expression in embryonal rhabdomyosarcoma suggests an origin in muscle satellite cells. Br J Cancer 2003; 89: 327–332. DOI: 10.1038/sj.bjc.6601040
45. Hettmer S, Liu J, Miller CM, Lindsay MC, Sparks CA, Guertin DA et al. Sarcomas induced in discrete subsets of prospectively isolated skeletal muscle cells. Proc Natl Acad Sci USA 2011; 108: 20002–20007. DOI: 10.1073/pnas.1111733108
46. Rubin BP, Nishijo K, Chen HI, Yi X, Schuetze DP, Pal R et al. Evidence for an unanticipated relationship between undifferentiated pleomorphic sarcoma and embryonal rhabdomyosarcoma. Cancer Cell 2011; 19: 177–191. DOI: 10.1016/j.ccr.2010.12.023
47. Asakura A, Hirai H, Kablar B, Morita S, Ishibashi J, Piras BA et al. Increased survival of muscle stem cells lacking the MyoD gene after transplantation into regenerating skeletal muscle. Proc Natl Acad Sci USA 2007; 104: 16552–16557. DOI: 10.1073/pnas.0708145104
48. Hirai H, Verma M, Watanabe S, Tastad C, Asakura Y, Asakura A. MyoD regulates apoptosis of myoblasts through microRNA-mediated down-regulation of Pax3. J Cell Biol 2010; 191: 347–365. DOI: 10.1083/jcb.201006025
49. Lepper C, Conway SJ, Fan CM. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 2009; 460: 627–631. DOI: 10.1038/nature08209
50. Vokes SA, Ji H, McCuine S, Tenzen T, Giles S, Zhong S et al. Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development 2007; 134: 1977–1989. DOI: 10.1242/dev.001966
51. Kimura H, Stephen D, Joyner A, Curran T. Gli1 is important for medulloblastoma formation in Ptc1+/- mice. Oncogene 2005; 24: 4026–4036. DOI: 10.1038/sj.onc.1208567
52. Vokes SA, Ji H, Wong WH, McMahon AP. A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev 2008; 22: 2651–2663. DOI: 10.1101/gad.1693008
53. 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: 423–434. DOI: 10.1016/S0092-8674(00)80678-9
54. Lauth M, Bergstrom A, Shimokawa T, Toftgard R. Inhibition of GLI-mediated transcription and tumor cell growth by small-molecule antagonists. Proc Natl Acad Sci USA 2007; 104: 8455–8460. DOI: 10.1073/pnas.0609699104
55. Brennan DJ, Ek S, Doyle E, Drew T, Foley M, Flannelly G et al. The transcription factor Sox11 is a prognostic factor for improved recurrence-free survival in epithelial ovarian cancer. Eur J Cancer 2009; 45: 1510–1517. DOI: 10.1016/j.ejca.2009.01.028
56. Liao YL, Sun YM, Chau GY, Chau YP, Lai TC, Wang JL et al. Identification of SOX4 target genes using phylogenetic footprinting-based prediction from expression microarrays suggests that overexpression of SOX4 potentiates metastasis in hepatocellular carcinoma. Oncogene 2008; 27: 5578–5589. DOI: 10.1038/onc.2008.168
57. Liu P, Ramachandran S, Ali Seyed M, Scharer CD, Laycock N, Dalton WB et al. Sex-determining region Y box 4 is a transforming oncogene in human prostate cancer cells. Cancer Res 2006; 66: 4011–4019. DOI: 10.1158/0008-5472.CAN-05-3055
58. Medina PP, Castillo SD, Blanco S, Sanz-Garcia M, Largo C, Alvarez S et al. The SRY-HMG box gene, SOX4, is a target of gene amplification at chromosome 6p in lung cancer. Hum Mol Genet 2009; 18: 1343–1352. DOI: 10.1093/hmg/ddp034
59. Kasper M, Jaks V, Are A, Bergstrom A, Schwager A, Barker N et al. Wounding enhances epidermal tumorigenesis by recruiting hair follicle keratinocytes. Proc Natl Acad Sci USA 2011; 108: 4099–4104. DOI: 10.1073/pnas.1014489108
60. Hatley ME, Tang W, Garcia MR, Finkelstein D, Millay DP, Liu N et al. A mouse model of rhabdomyosarcoma originating from the adipocyte lineage. Cancer Cell 2012; 22: 536–546. DOI: 10.1016/j.ccr.2012.09.004
61. Koleva M, Kappler R, Vogler M, Herwig A, Fulda S, Hahn H. Pleiotropic effects of sonic hedgehog on muscle satellite cells. Cell Mol Life Sci 2005; 62: 1863–1870. DOI: 10.1007/s00018-005-5072-9
62. Tostar U, Toftgard R, Zaphiropoulos PG, Shimokawa T. Reduction of human embryonal rhabdomyosarcoma tumor growth by inhibition of the hedgehog signaling pathway. Genes Cancer 2010; 1: 941–951. DOI: 10.1177/1947601910385449
63. Bhattaram P, Penzo-Mendez A, Sock E, Colmenares C, Kaneko KJ, Vassilev A et al. Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors. Nat Commun 2010; 1: 1–12. DOI: 10.1038/ncomms1008
64. Lee CJ, Appleby VJ, Orme AT, Chan WI, Scotting PJ. Differential expression of SOX4 and SOX11 in medulloblastoma. J Neurooncol 2002; 57: 201–214. DOI: 10.1023/A:1015773818302
65. Gerber AN, Wilson CW, Li YJ, Chuang PT. The hedgehog regulated oncogenes Gli1 and Gli2 block myoblast differentiation by inhibiting MyoD-mediated transcriptional activation. Oncogene 2007; 26: 1122–1136. DOI: 10.1038/sj.onc.1209891