A Mouse Model of Rhabdomyosarcoma Originating from the Adipocyte Lineage

Cancer Cell

Volumn 22, Issue 4, 2012, Pages 536-546

  Hatley, Mark E ^a,b,c   Tang, Wei ^a   Garcia, Matthew R ^a,b,c   Finkelstein, David ^c   Millay, Douglas P ^a   Liu, Ning ^a   Graff, Jonathan ^a   Galindo, Rene L ^a,b   Olson, Eric N ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN PRECURSOR; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN;

ADIPOCYTE; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER MODEL; CELL LINEAGE; CONTROLLED STUDY; EMBRYONAL RHABDOMYOSARCOMA; GENE EXPRESSION; HUMAN; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PENETRANCE; PRIORITY JOURNAL; PROADIPOCYTE;

EID: 84867596741     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2012.09.004     Document Type: Article

References (63)

1. Aguirre A.J., Bardeesy N., Sinha M., Lopez L., Tuveson D.A., Horner J., Redston M.S., DePinho R.A. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev. 2003, 17:3112-3126.
2. Atit R., Sgaier S.K., Mohamed O.A., Taketo M.M., Dufort D., Joyner A.L., Niswander L., Conlon R.A. Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Dev. Biol. 2006, 296:164-176.
3. Barlow C., Schroeder M., Lekstrom-Himes J., Kylefjord H., Deng C.X., Wynshaw-Boris A., Spiegelman B.M., Xanthopoulos K.G. Targeted expression of Cre recombinase to adipose tissue of transgenic mice directs adipose-specific excision of loxP-flanked gene segments. Nucleic Acids Res. 1997, 25:2543-2545.
4. Barr F.G. Gene fusions involving PAX and FOX family members in alveolar rhabdomyosarcoma. Oncogene 2001, 20:5736-5746.
5. Barr F.G., Womer R.B. Rhabdomyosarcoma. Oncology of Infancy and Childhood 2009, 743-781. Saunders, Philadelphia. S.H. Orkin, D.E. Fisher, A.T. Look, S.E. Lux, D. Ginsburg, D.G. Nathan (Eds.).
6. Beroukhim R., Mermel C.H., Porter D., Wei G., Raychaudhuri S., Donovan J., Barretina J., Boehm J.S., Dobson J., Urashima M., et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010, 463:899-905.
7. Bignell G.R., Greenman C.D., Davies H., Butler A.P., Edkins S., Andrews J.M., Buck G., Chen L., Beare D., Latimer C., et al. Signatures of mutation and selection in the cancer genome. Nature 2010, 463:893-898.
8. Brüning J.C., Michael M.D., Winnay J.N., Hayashi T., Hörsch D., Accili D., Goodyear L.J., Kahn C.R. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol. Cell 1998, 2:559-569.
9. Chen Y., Takita J., Mizuguchi M., Tanaka K., Ida K., Koh K., Igarashi T., Hanada R., Tanaka Y., Park M.J., Hayashi Y. Mutation and expression analyses of the MET and CDKN2A genes in rhabdomyosarcoma with emphasis on MET overexpression. Genes Chromosomes Cancer 2007, 46:348-358.
10. Corcoran R.B., Scott M.P. A mouse model for medulloblastoma and basal cell nevus syndrome. J. Neurooncol. 2001, 53:307-318.
11. Cypess A.M., Lehman S., Williams G., Tal I., Rodman D., Goldfine A.B., Kuo F.C., Palmer E.L., Tseng Y.H., Doria A., et al. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 2009, 360:1509-1517.
12. El-Badry O.M., Minniti C., Kohn E.C., Houghton P.J., Daughaday W.H., Helman L.J. Insulin-like growth factor II acts as an autocrine growth and motility factor in human rhabdomyosarcoma tumors. Cell Growth Differ. 1990, 1:325-331.
13. Engleka K.A., Gitler A.D., Zhang M., Zhou D.D., High F.A., Epstein J.A. Insertion of Cre into the Pax3 locus creates a new allele of Splotch and identifies unexpected Pax3 derivatives. Dev. Biol. 2005, 280:396-406.
14. Estep A.L., Tidyman W.E., Teitell M.A., Cotter P.D., Rauen K.A. HRAS mutations in Costello syndrome: detection of constitutional activating mutations in codon 12 and 13 and loss of wild-type allele in malignancy. Am. J. Med. Genet. A. 2006, 140:8-16.
15. Fan C.M., Tessier-Lavigne M. Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell 1994, 79:1175-1186.
16. Fukada S., Uezumi A., Ikemoto M., Masuda S., Segawa M., Tanimura N., Yamamoto H., Miyagoe-Suzuki Y., Takeda S. Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 2007, 25:2448-2459.
17. Galindo R.L., Allport J.A., Olson E.N. A Drosophila model of the rhabdomyosarcoma initiator PAX7-FKHR. Proc. Natl. Acad. Sci. USA 2006, 103:13439-13444.
18. Gattenloehner S., Vincent A., Leuschner I., Tzartos S., Müller-Hermelink H.K., Kirchner T., Marx A. The fetal form of the acetylcholine receptor distinguishes rhabdomyosarcomas from other childhood tumors. Am. J. Pathol. 1998, 152:437-444.
19. Glüer S., Schelp C., von Schweinitz D., Gerardy-Schahn R. Polysialylated neural cell adhesion molecule in childhood rhabdomyosarcoma. Pediatr. Res. 1998, 43:145-147.
20. Hahn H., Wojnowski L., Specht K., Kappler R., Calzada-Wack J., Potter D., Zimmer A., Müller U., Samson E., Quintanilla-Martinez L., Zimmer A. Patched target Igf2 is indispensable for the formation of medulloblastoma and rhabdomyosarcoma. J. Biol. Chem. 2000, 275:28341-28344.
21. He W., Barak Y., Hevener A., Olson P., Liao D., Le J., Nelson M., Ong E., Olefsky J.M., Evans R.M. Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc. Natl. Acad. Sci. USA 2003, 100:15712-15717.
22. Hettmer S., Wagers A.J. Muscling in: uncovering the origins of rhabdomyosarcoma. Nat. Med. 2010, 16:171-173.
23. Hettmer S., Liu J., Miller C.M., Lindsay M.C., Sparks C.A., Guertin D.A., Bronson R.T., Langenau D.M., Wagers A.J. Sarcomas induced in discrete subsets of prospectively isolated skeletal muscle cells. Proc. Natl. Acad. Sci. USA 2011, 108:20002-20007.
24. Heyn R., Newton W.A., Raney R.B., Hamoudi A., Bagwell C., Vietti T., Wharam M., Gehan E., Maurer H.M. Preservation of the bladder in patients with rhabdomyosarcoma. J. Clin. Oncol. 1997, 15:69-75.
25. Iolascon A., Faienza M.F., Coppola B., Rosolen A., Basso G., Della Ragione F., Schettini F. Analysis of cyclin-dependent kinase inhibitor genes (CDKN2A, CDKN2B, and CDKN2C) in childhood rhabdomyosarcoma. Genes Chromosomes Cancer 1996, 15:217-222.
26. Ishiguro N., Motoi T., Araki N., Ito H., Moriyama M., Yoshida H. Expression of cardiac ankyrin repeat protein, CARP, in malignant tumors: diagnostic use of CARP protein immunostaining in rhabdomyosarcoma. Hum. Pathol. 2008, 39:1673-1679.
27. Johnson R.A., Wright K.D., Poppleton H., Mohankumar K.M., Finkelstein D., Pounds S.B., Rand V., Leary S.E., White E., Eden C., et al. Cross-species genomics matches driver mutations and cell compartments to model ependymoma. Nature 2010, 466:632-636.
28. Johnson R.L., Laufer E., Riddle R.D., Tabin C. Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites. Cell 1994, 79:1165-1173.
29. Johnson R.L., Rothman A.L., Xie J., Goodrich L.V., Bare J.W., Bonifas J.M., Quinn A.G., Myers R.M., Cox D.R., Epstein E.H., Scott M.P. Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 1996, 272:1668-1671.
30. Kajimura S., Seale P., Kubota K., Lunsford E., Frangioni J.V., Gygi S.P., Spiegelman B.M. Initiation of myoblast to brown fat switch by a PRDM16-C/EBP-beta transcriptional complex. Nature 2009, 460:1154-1158.
31. Keller C., Capecchi M.R. New genetic tactics to model alveolar rhabdomyosarcoma in the mouse. Cancer Res. 2005, 65:7530-7532.
32. Lee Y., Kawagoe R., Sasai K., Li Y., Russell H.R., Curran T., McKinnon P.J. Loss of suppressor-of-fused function promotes tumorigenesis. Oncogene 2007, 26:6442-6447.
33. Lepper C., Conway S.J., Fan C.M. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 2009, 460:627-631.
34. Li F.P., Fraumeni J.F. Rhabdomyosarcoma in children: epidemiologic study and identification of a familial cancer syndrome. J. Natl. Cancer Inst. 1969, 43:1365-1373.
35. Li S., Czubryt M.P., McAnally J., Bassel-Duby R., Richardson J.A., Wiebel F.F., Nordheim A., Olson E.N. Requirement for serum response factor for skeletal muscle growth and maturation revealed by tissue-specific gene deletion in mice. Proc. Natl. Acad. Sci. USA 2005, 102:1082-1087.
36. Lum L., Beachy P.A. The hedgehog response network: sensors, switches, and routers. Science 2004, 304:1755-1759.
37. Mao J., Ligon K.L., Rakhlin E.Y., Thayer S.P., Bronson R.T., Rowitch D., McMahon A.P. A novel somatic mouse model to survey tumorigenic potential applied to the hedgehog pathway. Cancer Res. 2006, 66:10171-10178.
38. Münsterberg A.E., Kitajewski J., Bumcrot D.A., McMahon A.P., Lassar A.B. Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev. 1995, 9:2911-2922.
39. Paulson V., Chandler G., Rakheja D., Galindo R.L., Wilson K., Amatruda J.F., Cameron S. High-resolution array CGH identifies common mechanisms that drive embryonal rhabdomyosarcoma pathogenesis. Genes Chromosomes Cancer 2011, 50:397-408.
40. Pressey J.G., Anderson J.R., Crossman D.K., Lynch J.C., Barr F.G. Hedgehog pathway activity in pediatric embryonal rhabdomyosarcoma and undifferentiated sarcoma: a report from the Children's Oncology Group. Pediatr. Blood Cancer 2011, 57:930-938.
41. Rezvani G., Lui J.C., Barnes K.M., Baron J. A set of imprinted genes required for normal body growth also promotes growth of rhabdomyosarcoma cells. Pediatr. Res. 2012, 71:32-38.
42. Ross S.R., Graves R.A., Greenstein A., Platt K.A., Shyu H.L., Mellovitz B., Spiegelman B.M. A fat-specific enhancer is the primary determinant of gene expression for adipocyte P2 in vivo. Proc. Natl. Acad. Sci. USA 1990, 87:9590-9594.
43. Ross S.R., Choy L., Graves R.A., Fox N., Solevjeva V., Klaus S., Ricquier D., Spiegelman B.M. Hibernoma formation in transgenic mice and isolation of a brown adipocyte cell line expressing the uncoupling protein gene. Proc. Natl. Acad. Sci. USA 1992, 89:7561-7565.
44. Rubin B.P., Nishijo K., Chen H.I., Yi X., Schuetze D.P., Pal R., Prajapati S.I., Abraham J., Arenkiel B.R., Chen Q.R., et al. Evidence for an unanticipated relationship between undifferentiated pleomorphic sarcoma and embryonal rhabdomyosarcoma. Cancer Cell 2011, 19:177-191.
45. Seale P., Rudnicki M.A. A new look at the origin, function, and "stem-cell" status of muscle satellite cells. Dev. Biol. 2000, 218:115-124.
46. Seale P., Bjork B., Yang W., Kajimura S., Chin S., Kuang S., Scimè A., Devarakonda S., Conroe H.M., Erdjument-Bromage H., et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature 2008, 454:961-967.
47. Shadrach J.L., Wagers A.J. Stem cells for skeletal muscle repair. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2011, 366:2297-2306.
48. Sharp R., Recio J.A., Jhappan C., Otsuka T., Liu S., Yu Y., Liu W., Anver M., Navid F., Helman L.J., et al. Synergism between INK4a/ARF inactivation and aberrant HGF/SF signaling in rhabdomyosarcomagenesis. Nat. Med. 2002, 8:1276-1280.
49. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
50. Spunt S.L., Lobe T.E., Pappo A.S., Parham D.M., Wharam M.D., Arndt C., Anderson J.R., Crist W.M., Paidas C., Wiener E., et al. Aggressive surgery is unwarranted for biliary tract rhabdomyosarcoma. J. Pediatr. Surg. 2000, 35:309-316.
51. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
52. Suh J.M., Gao X., McKay J., McKay R., Salo Z., Graff J.M. Hedgehog signaling plays a conserved role in inhibiting fat formation. Cell Metab. 2006, 3:25-34.
53. Tallquist M.D., Weismann K.E., Hellström M., Soriano P. Early myotome specification regulates PDGFA expression and axial skeleton development. Development 2000, 127:5059-5070.
54. Tang W., Zeve D., Suh J.M., Bosnakovski D., Kyba M., Hammer R.E., Tallquist M.D., Graff J.M. White fat progenitor cells reside in the adipose vasculature. Science 2008, 322:583-586.
55. Tiffin N., Williams R.D., Shipley J., Pritchard-Jones K. PAX7 expression in embryonal rhabdomyosarcoma suggests an origin in muscle satellite cells. Br. J. Cancer 2003, 89:327-332.
56. Tostar U., Malm C.J., Meis-Kindblom J.M., Kindblom L.G., Toftgård R., Undén A.B. 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.
57. Urs S., Harrington A., Liaw L., Small D. Selective expression of an aP2/Fatty Acid Binding Protein 4-Cre transgene in non-adipogenic tissues during embryonic development. Transgenic Res. 2006, 15:647-653.
58. van Marken Lichtenbelt W.D., Vanhommerig J.W., Smulders N.M., Drossaerts J.M., Kemerink G.J., Bouvy N.D., Schrauwen P., Teule G.J. Cold-activated brown adipose tissue in healthy men. N. Engl. J. Med. 2009, 360:1500-1508.
59. Virtanen K.A., Lidell M.E., Orava J., Heglind M., Westergren R., Niemi T., Taittonen M., Laine J., Savisto N.J., Enerbäck S., Nuutila P. Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 2009, 360:1518-1525.
60. Wang Q., Fang W.H., Krupinski J., Kumar S., Slevin M., Kumar P. Pax genes in embryogenesis and oncogenesis. J. Cell. Mol. Med. 2008, 12(6A):2281-2294.
61. Williamson D., Missiaglia E., de Reyniès A., Pierron G., Thuille B., Palenzuela G., Thway K., Orbach D., Laé M., Fréneaux P., et al. Fusion gene-negative alveolar rhabdomyosarcoma is clinically and molecularly indistinguishable from embryonal rhabdomyosarcoma. J. Clin. Oncol. 2010, 28:2151-2158.
62. Yamamoto M., Shook N.A., Kanisicak O., Yamamoto S., Wosczyna M.N., Camp J.R., Goldhamer D.J. A multifunctional reporter mouse line for Cre- and FLP-dependent lineage analysis. Genesis 2009, 47:107-114.
63. Zibat A., Missiaglia E., Rosenberger A., Pritchard-Jones K., Shipley J., Hahn H., Fulda S. Activation of the hedgehog pathway confers a poor prognosis in embryonal and fusion gene-negative alveolar rhabdomyosarcoma. Oncogene 2010, 29:6323-6330.