Cavin-1 and Caveolin-1 are both required to support cell proliferation, migration and anchorage-independent cell growth in rhabdomyosarcoma

Laboratory Investigation

Volumn 95, Issue 6, 2015, Pages 585-602

  Faggi, Fiorella ^a,b   Chiarelli, Nicola ^a   Colombi, Marina ^a   Mitola, Stefania ^a   Ronca, Roberto ^a   Madaro, Luca ^b,c   Bouche, Marina ^b,c   Poliani, Pietro L ^a   Vezzoli, Marika ^a   Longhena, Francesca ^a   Monti, Eugenio ^a   Salani, Barbara ^d   Maggi, Davide ^d   Keller, Charles ^e,f   Fanzani, Alessandro ^a,b  

^a UNIVERSITY OF BRESCIA   (Italy)

^b Interuniversity Institute of Myology   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^f Children's Cancer Therapy Development Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CAVEOLIN 1; CAVIN 1; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; PTRF PROTEIN, HUMAN; PTRF PROTEIN, MOUSE; RNA BINDING PROTEIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAVEOLA; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHILDHOOD CANCER; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; HUMAN; HUMAN CELL; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RHABDOMYOSARCOMA; SOFT TISSUE TUMOR; ANIMAL; CELL CULTURE; CELL MOTION; GENE SILENCING; GENETICS; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE SATELLITE CELL; TUMOR CELL LINE;

ANIMALS; CAVEOLIN 1; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; MEMBRANE PROTEINS; MICE; RHABDOMYOSARCOMA; RNA-BINDING PROTEINS; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84930021783     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2015.45     Document Type: Article

References (106)

1. Parham DM, Alaggio R, Coffin CM. Myogenic tumors in children and adolescents. Pediatr Dev Pathol 2012; 15: 211-238
2. Keller C, Guttridge DC. Mechanisms of impaired differentiation in rhabdomyosarcoma. FEBS J 2013; 280: 4323-4334
3. Zanola A, Rossi S, Faggi F, et al. Rhabdomyosarcomas: an overview on the experimental animal models. J Cell Mol Med 2012; 16: 1377-1391
4. Tiffin N, Williams RD, Shipley J, et al. PAX7 expression in embryonal rhabdomyosarcoma suggests an origin in muscle satellite cells. Br J Cancer 2003; 89: 327-332
5. Morotti RA, Nicol KK, Parham DM, et al. An immunohistochemical algorithm to facilitate diagnosis and subtyping of rhabdomyosarcoma: the children's oncology group experience. Am J Surg Pathol 2006; 30: 962-968
6. Ren YX, Finckenstein FG, Abdueva DA, et al. Mouse mesenchymal stem cells expressing PAX-FKHR form alveolar rhabdomyosarcomas by cooperating with secondary mutations. Cancer Res 2008; 68: 6587-6597
7. Charytonowicz E, Cordon-Cardo C, Matushansky I, et al. Alveolar rhabdomyosarcoma: is the cell of origin a mesenchymal stem cell? Cancer Lett 2009; 279: 126-136
8. Hettmer S, Liu J, Miller CM, et al. Sarcomas induced in discrete subsets of prospectively isolated skeletal muscle cells. Proc Natl Acad Sci USA 2011; 108: 20002-20007
9. Linardic CM, Downie DL, Qualman S, et al. Genetic modeling of human rhabdomyosarcoma. Cancer Res 2005; 65: 4490-4495
10. Rubin BP, Nishijo K, Chen HI, et al. Evidence for an unanticipated relationship between undifferentiated pleomorphic sarcoma and embryonal rhabdomyosarcoma. Cancer Cell 2011; 19: 177-191
11. Langenau DM, Keefe MD, Storer NY, et al. Effects of RAS on the genesis of embryonal rhabdomyosarcoma. Genes Dev 2007; 21: 1382-1395
12. Keller C, Capecchi MR. New genetic tactics to model alveolar rhabdomyosarcoma in the mouse. Cancer Res 2005; 65: 7530-7532
13. Keller C, Arenkiel BR, Coffin CM, et al. Alveolar rhabdomyosarcomas in conditional Pax3: Fkhr mice: cooperativity of Ink4a/ARF and Trp53 loss of function. Genes Dev 2004; 18: 2614-2626
14. Abraham J, Nuñez-Álvarez Y, Hettmer S, et al. Lineage of origin in rhabdomyosarcoma informs pharmacological response. Genes Dev 2014; 28: 1578-1591
15. Hatley ME, Tang W, Garcia MR, et al. A mouse model of rhabdomyosarcoma originating from the adipocyte lineage. Cancer Cell 2012; 22: 536-546
16. Wolden SL, Alektiar KM. Sarcomas across the age spectrum. Semin Radiat Oncol 2010; 20: 45-51
17. Abraham J, Prajapati SI, Nishijo K, et al. Evasion mechanisms to Igf1r inhibition in rhabdomyosarcoma. Mol Cancer Ther 2011; 10: 697-707
18. Ayalon D, Glaser T, Werner H. Transcriptional regulation of IGF-I receptor gene expression by the PAX3-FKHR oncoprotein. Growth Horm IGF Res 2001; 11: 289-297
19. Rikhof B, de Jong S, Suurmeijer AJ, et al. The insulin-like growth factor system and sarcomas. J Pathol 2009; 217: 469-482
20. Taylor JG, Cheuk AT, Tsang PS, et al. Identification of FGFR4-Activating mutations in human rhabdomyosarcomas that promote metastasis in xenotransplanted models. J Clin Invest 2009; 119: 3395-3407
21. Shern JF, Chen L, Chmielecki J, et al. Comprehensive genomic analysis of rhabdomyosarcoma reveals a landscape of alterations affecting a common genetic axis in fusion-positive and fusion-negative tumors. Cancer Discov 2014; 4: 216-231
22. Lee Y, Kawagoe R, Sasai K, et al. Loss of suppressor-of-fused function promotes tumorigenesis. Oncogene 2007; 26: 6442-6447
23. Donehower LA, Harvey M, Slagle BL, et al. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992; 356: 215-221
24. Kohashi K, Oda Y, Yamamoto H, et al. Alterations of RB1 gene in embryonal and alveolar rhabdomyosarcoma: special reference to utility of pRB immunoreactivity in differential diagnosis of rhabdomyosarcoma subtype. J Cancer Res Clin Oncol 2008; 134: 1097-1103
25. Chamberlain JS, Metzger J, Reyes M, et al. Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J 2007; 21: 2195-2204
26. Fernandez K, Serinagaoglu Y, Hammond S, et al. Mice lacking dystrophin or alpha sarcoglycan spontaneously develop embryonal rhabdomyosarcoma with cancer-Associated p53 mutations and alternatively spliced or mutant Mdm2 transcripts. Am J Pathol 2010; 176: 416-434
27. Hosur V, Kavirayani A, Riefler J, et al. Dystrophin and dysferlin double mutant mice: a novel model for rhabdomyosarcoma. Cancer Genet 2012; 205: 232-241
28. Wang Y, Marino-Enriquez A, Bennett RR, et al. Dystrophin is a tumor suppressor in human cancers with myogenic programs. Nat Genet 2014; 46: 601-606
29. Schmidt WM, Uddin MH, Dysek S, et al. DNA damage, somatic aneuploidy, and malignant sarcoma susceptibility in muscular dystrophies. PLoS Genet 2011; 7: e1002042
30. Fanzani A, Monti E, Donato R, et al. Muscular dystrophies share pathogenetic mechanisms with muscle sarcomas. Trends Mol Med 2013; 19: 546-554
31. Galili N, Davis RJ, Fredericks WJ, et al. Fusion of a fork head domain gene to PAX3 in the solid tumour alveolar rhabdomyosarcoma. Nat Genet 1993; 5: 230-235
32. Barr FG, Galili N, Holick J, et al. Rearrangement of the PAX3 paired box gene in the paediatric solid tumour alveolar rhabdomyosarcoma. Nat Genet 1993; 3: 113-117
33. Davis RJ, D'Cruz CM, Lovell MA, et al. Fusion of PAX7 to FKHR by the variant t(1; 13)(p36; q14) translocation in alveolar rhabdomyosarcoma. Cancer Res 1994; 54: 2869-2872
34. Graf Finckenstein F, Shahbazian V, Davicioni E, et al. PAX-FKHR function as pangenes by simultaneously inducing and inhibiting myogenesis. Oncogene 2008; 27: 2004-2014
35. Keller C, Hansen MS, Coffin CM, et al. Pax3: Fkhr interferes with embryonic Pax3 and Pax7 function: implications for alveolar rhabdomyosarcoma cell of origin. Genes Dev 2004; 18: 2608-2613
36. Kikuchi K, Hettmer S, Aslam MI, et al. Cell-cycle dependent expression of a translocation-mediated fusion oncogene mediates checkpoint adaptation in rhabdomyosarcoma. PLoS Genet 2014; 10: e1004107
37. Parton RG, del Pozo MA. Caveolae as plasma membrane sensors, protectors and organizers. Nat Rev Mol Cell Biol 2013; 14: 98-112
38. Williams TM, Lisanti MP. The caveolin proteins. Genome Biol 2004; 5: 214
39. Razani B, Woodman SE, Lisanti MP. Caveolae: from cell biology to animal physiology. Pharmacol Rev 2002; 54: 431-467
40. Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol 2007; 8: 185-194
41. Nabi IR. Cavin fever: regulating caveolae. Nat Cell Biol 2009; 11: 789-791
42. Hansen CG, Nichols BJ. Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 2010; 20: 177-186
43. Hayer A, Stoeber M, Bissig C, et al. Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic 2010; 11: 361-382
44. Briand N, Dugail I, Le Lay S. Cavin proteins: new players in the caveolae field. Biochimie 2011; 93: 71-77
45. Drab M, Verkade P, Elger M, et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 genedisrupted mice. Science 2001; 293: 2449-2452
46. Hill MM, Bastiani M, Luetterforst R, et al. PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 2008; 132: 113-124
47. Liu L, Pilch PF. A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J Biol Chem 2008; 283: 4314-4322
48. Liu L, Brown D, McKee M, et al. Deletion of Cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell Metab 2008; 8: 310-317
49. Fra AM, Williamson E, Simons K, et al. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci USA 1995; 92: 8655-8659
50. Walser PJ, Ariotti N, Howes M, et al. Constitutive formation of caveolae in a bacterium. Cell 2012; 150: 752-763
51. Hansen CG, Shvets E, Howard G, et al. Deletion of cavin genes reveals tissue-specific mechanisms for morphogenesis of endothelial caveolae. Nat Commun 2013; 4: 1831
52. Rossi S, Poliani PL, Cominelli M, et al. Caveolin 1 is a marker of poor differentiation in rhabdomyosarcoma. Eur J Cancer 2011; 47: 761-772
53. Rossi S, Poliani PL, Missale C, et al. Caveolins in rhabdomyosarcoma. J Cell Mol Med 2011; 15: 2553-2568
54. Faggi F, Mitola S, Sorci G, et al. Phosphocaveolin-1 enforces tumor growth and chemoresistance in rhabdomyosarcoma. PLoS One 2014; 9: e84618
55. Irizarry RA, Hobbs B, Collin F, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4: 249-264
56. Madaro L, Marrocco V, Fiore P, et al. PKC? signaling is required for myoblast fusion by regulating the expression of caveolin-3 and ?1D integrin upstream focal adhesion kinase. Mol Biol Cell 2011; 22: 1409-1419
57. Houghton JA, Houghton PJ, Brodeur GM, et al. Development of resistance to vincristine in a childhood rhabdomyosarcoma growing in immune-deprived mice. Int J Cancer 1981; 28: 409-415
58. Stratton MR, Fisher C, Gusterson BA, et al. Detection of point mutations in N-ras and K-ras genes of human embryonal rhabdomyosarcomas using oligonucleotide probes and the polymerase chain reaction. Cancer Res 1989; 49: 6324-6327
59. Felix CA, Kappel CC, Mitsudomi T, et al. Frequency and diversity of p53 mutations in childhood rhabdomyosarcoma. Cancer Res 1992; 52: 2243-2247
60. Lollini PL, De Giovanni C, Landuzzi L, et al. Reduced metastatic ability of in vitro differentiated human rhabdomyosarcoma cells. Invasion Metastasis 1991; 11: 116-124
61. Astolfi A, De Giovanni C, Landuzzi L, et al. Identification of new genes related to the myogenic differentiation arrest of human rhabdomyosarcoma cells. Gene 2001; 274: 139-149
62. Douglass EC, Valentine M, Etcubanas E, et al. A specific chromosomal abnormality in rhabdomyosarcoma. Cytogenet Cell Genet 1987; 45: 148-155
63. Borenfreund E, Puerner JA. Toxicity determined in vitro by morphological alterations and neutral red absorption. Toxicol Lett 1985; 24: 119-124
64. Repetto G, del Peso A, Zurita JL. Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc 2008; 3: 1125-1131
65. Pannérec A, Marazzi G, Sassoon D. Stem cells in the hood: the skeletal muscle niche. Trends Mol Med 2012; 18: 599-606
66. Marampon F, Ciccarelli C, Zani BM. Down-regulation of c-Myc following MEK/ERK inhibition halts the expression of malignant phenotype in rhabdomyosarcoma and in non muscle-derived human tumors. Mol Cancer 2006; 5: 31
67. Marampon F, Bossi G, Ciccarelli C, et al. MEK/ERK inhibitor U0126 affects in vitro and in vivo growth of embryonal rhabdomyosarcoma. Mol Cancer Ther 2009; 8: 543-551
68. D?bro? W, Adamczyk A, Ciurkot K, et al. Vanadium compounds affect growth and morphology of human rhabdomyosarcoma cell line. Pol J Pathol 2011; 62: 262-268
69. Hayer A, Stoeber M, Ritz D, et al. Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation. J Cell Biol 2010; 191: 615-629
70. Detzer A, Engel C, Wünsche W, et al. Cell stress is related to relocalization of Argonaute 2 and to decreased RNA interference in human cells. Nucleic Acids Res 2011; 39: 2727-2741
71. Jansa P, Mason SW, Hoffmann-Rohrer U, et al. Cloning and functional characterization of PTRF, a novel protein which induces dissociation of paused ternary transcription complexes. EMBO J 1998; 17: 2855-2864
72. Jansa P, Burek C, Sander EE, et al. The transcript release factor PTRF augments ribosomal gene transcription by facilitating reinitiation of RNA polymerase I. Nucleic Acids Res 2001; 29: 423-429
73. Hasegawa T, Takeuchi A, Miyaishi O, et al. PTRF (polymerase I and transcript-release factor) is tissue-specific and interacts with the BFCOL1 (binding factor of a type-I collagen promoter) zinc-finger transcription factor which binds to the two mouse type-I collagen gene promoters. Biochem J 2000; 347: 55-59
74. Foster LJ, De Hoog CL, Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci USA 2003; 100: 5813-5818
75. Vinten J, Voldstedlund M, Clausen H, et al. A 60-kDa protein abundant in adipocyte caveolae. Cell Tissue Res 2001; 305: 99-106
76. Aboulaich N, Vainonen JP, Strålfors P, et al. Vectorial proteomics reveal targeting, phosphorylation and specific fragmentation of polymerase I and transcript release factor (PTRF) at the surface of caveolae in human adipocytes. Biochem J 2004; 383: 237-248
77. Aboulaich N, Ortegren U, Vener AV, et al. Association and insulin regulated translocation of hormone-sensitive lipase with PTRF. Biochem Biophys Res Commun 2006; 350: 657-661
78. Aboulaich N, Chui PC, Asara JM, et al. Polymerase I and transcript release factor regulates lipolysis via a phosphorylation-dependent mechanism. Diabetes 2011; 60: 757-765
79. Dwianingsih EK, Takeshima Y, Itoh K, et al. A Japanese child with asymptomatic elevation of serum creatine kinase shows PTRF-CAVIN mutation matching with congenital generalized lipodystrophy type 4. Mol Genet Metab 2010; 101: 233-237
80. Hayashi YK, Matsuda C, Ogawa M, et al. Human PTRF mutations cause secondary deficiency of caveolins resulting in muscular dystrophy with generalized lipodystrophy. J Clin Invest 2009; 119: 2623-2633
81. Rajab A, Straub V, McCann LJ, et al. Fatal cardiac arrhythmia and long-QT syndrome in a new form of congenital generalized lipodystrophy with muscle rippling (CGL4) due to PTRF-CAVIN mutations. PLoS Genet 2010; 6: e1000874
82. Shastry S, Delgado MR, Dirik E, et al. Congenital generalized lipodystrophy, type 4 (CGL4) associated with myopathy due to novel PTRF mutations. Am J Med Genet A 2010; 152A: 2245-2253
83. Ardissone A, Bragato C, Caffi L, et al. Novel PTRF mutation in a child with mild myopathy and very mild congenital lipodystrophy. BMC Med Genet 2013; 14: 89
84. de Haan W. Lipodystrophy and muscular dystrophy caused by PTRF mutations. Clin Genet 2010; 77: 436-437
85. Ding SY, Lee MJ, Summer R, et al. Pleiotropic effects of cavin-1 deficiency on lipid metabolism. J Biol Chem 2014; 289: 8473-8483
86. Zhu H, Lin P, De G, et al. Polymerase transcriptase release factor (PTRF) anchors MG53 protein to cell injury site for initiation of membrane repair. J Biol Chem 2011; 286: 12820-12824
87. Bai L, Deng X, Li Q, et al. Down-regulation of the cavin family proteins in breast cancer. J Cell Biochem 2012; 113: 322-328
88. Gámez-Pozo A, Sánchez-Navarro I, Calvo E, et al. PTRF/cavin-1 and MIF proteins are identified as non-small cell lung cancer biomarkers by label-free proteomics. PLoS One 2012; 7: e33752
89. Aung CS, Hill MM, Bastiani M, et al. PTRF-cavin-1 expression decreases the migration of PC3 prostate cancer cells: role of matrix metalloprotease 9. Eur J Cell Biol 2011; 90: 136-142
90. Hill MM, Daud NH, Aung CS, et al. Co-regulation of cell polarization and migration by caveolar proteins PTRF/Cavin-1 and caveolin-1. PLoS One 2012; 7: e43041
91. Inder KL, Zheng YZ, Davis MJ, et al. Expression of PTRF in PC-3 cells modulates cholesterol dynamics and the actin cytoskeleton impacting secretion pathways. Mol Cell Proteomics 2012; 11: M111.012245
92. Moon H, Lee CS, Inder KL, et al. PTRF/cavin-1 neutralizes non-caveolar caveolin-1 microdomains in prostate cancer. Oncogene 2014; 33: 3561-3570
93. Nassar ZD, Moon H, Duong T, et al. PTRF/Cavin-1 decreases prostate cancer angiogenesis and lymphangiogenesis. Oncotarget 2013; 4: 1844-1855
94. Liu L, Xu HX, Wang WQ, et al. Cavin-1 is essential for the tumorpromoting effect of caveolin-1 and enhances its prognostic potency in pancreatic cancer. Oncogene 2013; 33: 2728-2736
95. Yi JS, Mun DG, Lee H, et al. PTRF/Cavin-1 is essential for multidrug resistance in cancer cells. J Proteome Res 2013; 12: 605-614
96. Williams TM, Lisanti MP. Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am J Physiol Cell Physiol 2005; 288: C494-C506
97. Burgermeister E, Liscovitch M, Röcken C, et al. Caveats of caveolin-1 in cancer progression. Cancer Lett 2008; 268: 187-201
98. Goetz JG, Lajoie P, Wiseman SM, et al. Caveolin-1 in tumor progression: the good, the bad and the ugly. Cancer Metastasis Rev 2008; 27: 715-735
99. Sáinz-Jaspeado M, Martin-Liberal J, Lagares-Tena L, et al. Caveolin-1 in sarcomas: friend or foe? Oncotarget 2011; 2: 305-312
100. Tirado OM, MacCarthy CM, Fatima N, et al. Caveolin-1 promotes resistance to chemotherapy-induced apoptosis in Ewing's sarcoma cells by modulating PKCalpha phosphorylation. Int J Cancer 2010; 126: 426-436
101. Gupta R, Toufaily C, Annabi B. Caveolin and cavin family members: dual roles in cancer. Biochimie 2014; 107: 188-202
102. Volonte D, Galbiati F. Polymerase I and transcript release factor (PTRF)/cavin-1 is a novel regulator of stress-induced premature senescence. J Biol Chem 2011; 286: 28657-28661
103. Bai L, Deng X, Li J, et al. Regulation of cellular senescence by the essential caveolar component PTRF/Cavin-1. Cell Res 2011; 21: 1088-1101
104. Salani B, Passalacqua M, Maffioli S, et al. IGF-IR internalizes with Caveolin-1 and PTRF/Cavin in HaCat cells. PLoS One 2010; 5: e14157
105. Hamoudane M, Maffioli S, Cordera R, et al. Caveolin-1 and polymerase I and transcript release factor: new players in insulin-like growth factor-I receptor signaling. J Endocrinol Invest 2013; 36: 204-208
106. Malkin D, Li FP, Strong LC, et al. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. Science 1990; 250: 1233-1238