Overactivation of Ras signaling pathway in CD133+ MPNST cells

Journal of Neuro-Oncology

Volumn 108, Issue 3, 2012, Pages 423-434

  Borrego Diaz, Emma ^a   Terai, Kaoru ^a   Lialyte, Kristina ^a   Wise, Amanda L ^a   Esfandyari, Tuba ^a   Behbod, Fariba ^a   Mautner, Victor F ^b   Spyra, Melanie ^b   Taylor, Sarah ^a   Parada, Luis F ^c   Upadhyaya, Meena ^d   Farassati, Faris ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

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

^d CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Cancer stem cells; CD133; Malignant peripheral nerve sheath tumor; Ral; Ras; Tumor initiating cells

Indexed keywords

BETA CATENIN; CD133 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PAXILLIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN IRE1; PROTEIN IRE1ALPHA; PROTEIN RALA; RAL PROTEIN; RAS PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER STEM CELL; CELL INVASION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; MALIGNANT PERIPHERAL NERVE SHEATH TUMOR; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FOLDING; SCHWANN CELL; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD; APOPTOSIS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; ENDOPLASMIC RETICULUM STRESS; FLOW CYTOMETRY; GLYCOPROTEINS; HUMANS; IMMUNOPHENOTYPING; MICE; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; NERVE SHEATH NEOPLASMS; PEPTIDES; RAS PROTEINS; SIGNAL TRANSDUCTION;

EID: 84864060471     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-012-0852-1     Document Type: Article

References (72)

1. Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414:105-111. doi:10.1038/ 35102167 (Pubitemid 33041634)
2. Bignold LP, Coghlan BL, Jersmann HP (2006) Hansemann, Boveri, chromosomes and the gametogenesis-related theories of tumours. Cell Biol Int 30:640-644. doi:10.1016/j.cellbi.2006.04. 002 (Pubitemid 44107723)
3. D'Amour KA, Gage FH (2002) Are somatic stem cells pluripo-tent or lineage-restricted? Nat Med 8:213-214. doi:10.1038/ nm0302-213
4. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432:396-401. doi: 10.1038/nature03128 (Pubitemid 39551674)
5. Akhtar K, Bussen W, Scott SP (2009) Cancer stem cells\-from initiation to elimination, how far have we reached? (review). Int J Oncol 34:1491-1503
6. Trosko JE (2009) Review paper: cancer stem cells and cancer nonstem cells: from adult stem cells or from reprogramming of differentiated somatic cells. Vet Pathol 46:176-193. doi:10.1354/ vp.46-2-176
7. Pan Y, Huang X (2008) Epithelial ovarian cancer stem cells\-a review. Int J Clin Exp Med 1:260-266
8. Sagar J, Chaib B, Sales K, Winslet M, Seifalian A (2007) Role of stem cells in cancer therapy and cancer stem cells: a review. Cancer Cell Int 7:9. doi:10.1186/1475-2867-7-9 (Pubitemid 47009117)
9. Spillane JB, Henderson MA (2007) Cancer stem cells: a review. ANZ J Surg 77:464-468. doi:10.1111/j.1445-2197.2007.04096.x (Pubitemid 46733809)
10. Costa FF, Le Blanc K, Brodin B (2007) Concise review: cancer/ testis antigens, stem cells, and cancer. Stem Cells 25:707-711. doi:10.1634/stemcells. 2006-0469 (Pubitemid 46354230)
11. Mimeault M, Batra SK (2006) Concise review: recent advances on the significance of stem cells in tissue regeneration and cancer therapies. Stem Cells 24:2319-2345. doi:10.1634/stemcells.2006-0066 (Pubitemid 44679695)
12. Meeker AK, Coffey DS (1997) Telomerase: a promising marker of biological immortality of germ, stem, and cancer cells. A review. Biochemistry 62:1323-1331 (Pubitemid 127665922)
13. Rudland PS, Ormerod EJ, Paterson FC (1980) Stem cells in rat mammary development and cancer: a review. J R Soc Med 73: 437-442 (Pubitemid 10010643)
14. Polyak K, Hahn WC (2006) Roots and stems: stem cells in cancer. Nat Med 12:296-300. doi:10.1038/nm1379 (Pubitemid 43355075)
15. Huntly BJ, Gilliland DG (2005) Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat Rev Cancer 5: 311-321. doi:10.1038/nrc1592 (Pubitemid 40488636)
16. Downward J (2003) Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 3:11-22 (Pubitemid 37328883)
17. Brannan CI, Perkins AS, Vogel KS, Ratner N, Nordlund ML, Reid SW, Buchberg AM, Jenkins NA, Parada LF, Copeland NG (1994) Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev 8:1019-1029 (Pubitemid 24145666)
18. Goldfinger LE (2008) Choose your own path: specificity in Ras GTPase signaling. Mol Biosyst 4:293-299 (Pubitemid 351422584)
19. Rajalingam K, Schreck R, Rapp UR, Albert S (2007) Ras oncogenes and their downstream targets. Biochim Biophys Acta 1773:1177-1195 (Pubitemid 47125979)
20. Giehl K (2005) Oncogenic Ras in tumour progression and metastasis. Biol Chem 386:193-205 (Pubitemid 40485425)
21. Harrisingh MC, Perez-Nadales E, Parkinson DB, Malcolm DS, Mudge AW, Lloyd AC (2004) The Ras/Raf/ERK signalling pathway drives Schwann cell dedifferentiation. EMBO J 23: 3061-3071 (Pubitemid 39093600)
22. Harrisingh MC, Lloyd AC (2004) Ras/Raf/ERK signalling and NF1. Cell Cycle 3(10):1255-1258
23. Bollag G, Clapp DW, Shih S, Adler F, Zhang YY, Thompson P, Lange BJ, Freedman MH, McCormick F, Jacks T, Shannon K (1996) Loss of NF1 results in activation of the Ras signaling pathway and leads to aberrant growth in haematopoietic cells. Nat Genet 12:144-148 (Pubitemid 26051293)
24. Hiatt KK, Ingram DA, Zhang Y, Bollag G, Clapp DW (2001) Neurofibromin GTPase-activating protein-related domains restore normal growth in Nf1?/\- cells. J Biol Chem 276:7240-7245
25. Basu TN, Gutmann DH, Fletcher JA, Glover TW, Collins FS, Downward J (1992) Aberrant regulation of Ras proteins in malignant tumour cells from type 1 neurofibromatosis patients. Nature 356:713-715
26. Lakkis MM, Tennekoon GI (2000) Neurofibromatosis type 1. I. General overview. J Neurosci Res 62:755-763
27. Upadhyaya M, Spurlock G, Majounie E, Griffiths S, Forrester N, Baser M, Huson SM, Gareth Evans D, Ferner R (2006) The heterogeneous nature of germline mutations in NF1 patients with malignant peripheral serve sheath tumours (MPNSTs). Hum Mutat 27:716
28. Ferner RE (2007) Neurofibromatosis 1. Eur J Hum Genet 15: 131-138 (Pubitemid 46111848)
29. Bodempudi V, Yamoutpoor F, Pan W, Dudek AZ, Esfandyari T, Piedra M, Babovick-Vuksanovic D, Woo RA, Mautner VF, Kluwe L, Clapp DW, De Vries GH, Thomas SL, Kurtz A, Parada LF, Farassati F (2009) Ral overactivation in malignant peripheral nerve sheath tumors. Mol Cell Biol 29:3964-3974
30. Menon AG, Anderson KM, Riccardi VM, Chung RY, Whaley JM, Yandell DW, Farmer GE, Freiman RN, Lee JK, Li FP (1990) Chromosome 17p deletions and p53 gene mutations associated with the formation of malignant neurofibrosarcomas in von Reckling-hausen neurofibromatosis. Proc Natl Acad Sci USA 87:5435-5439
31. Legius E, Dierick H, Wu R, Hall BK, Marynen P, Cassiman JJ, Glover TW (1994) TP53 mutations are frequent in malignant NF1 tumors. Genes Chromosomes Cancer 10:250-255 (Pubitemid 24238432)
32. Rey JA, Pestana A, Bello MJ (1992) Cytogenetics and molecular genetics of nervous system tumors. Oncol Res 4:321-331 (Pubitemid 23167116)
33. Farassati F, Yang AD, Lee PW (2001) Oncogenes in Ras sig-nalling pathway dictate host-cell permissiveness to herpes sim-plex virus 1. Nat Cell Biol 3:745-750 (Pubitemid 32734253)
34. Corbeil D, Fargeas CA, Huttner WB (2001) Rat prominin, like its mouse and human orthologues, is a pentaspan membrane glyco-protein. Biochem Biophys Res Commun 285:939-944. doi: 10.1006/bbrc.2001.5271 (Pubitemid 32918027)
35. Corbeil D, Roper K, Fargeas CA, Joester A, Huttner WB (2001) Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2:82-91 (Pubitemid 32219860)
36. Mehra N, Penning M, Maas J, Beerepoot LV, van Daal N, van Gils CH, Giles RH, Voest EE (2006) Progenitor marker CD133 mRNA is elevated in peripheral blood of cancer patients with bone metastases. Clin Cancer Res 12:4859-4866. doi:10.1158/ 1078-0432.CCR-06-0422 (Pubitemid 44338571)
37. Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, Holden JT, Bray RA, Waller EK, Buck DW (1997) A novel five-trans-membrane hematopoietic stem cell antigen: isolation, character-ization, and molecular cloning. Blood 90:5013-5021 (Pubitemid 28007218)
38. Salmaggi A, Boiardi A, Gelati M, Russo A, Calatozzolo C, Ci-usani E, Sciacca FL, Ottolina A, Parati EA, La Porta C, Aless-andri G, Marras C, Croci D, De Rossi M (2006) Glioblastoma-derived tumorospheres identify a population of tumor stem-like cells with angiogenic potential and enhanced multidrug resistance phenotype. Glia 54:850-860. doi:10.1002/glia.20414 (Pubitemid 44671990)
39. Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, Gritti A, Piccinini A, Porro D, Santinami M, In-vernici G, Parati E, Alessandri G, La Porta CA (2007) Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 43:935-946. doi:10.1016/ j.ejca.2007.01.017 (Pubitemid 46366698)
40. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immu-nodeficient mice. Nature 445:106-110. doi:10.1038/nature05372 (Pubitemid 46067310)
41. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumorigenic prostate cancer stem cells. CancerRes 65:10946-10951. doi:10.1158/0008-5472.CAN-05-2018 (Pubitemid 41713363)
42. Neuzil J, Stantic M, Zobalova R, Chladova J, Wang X, Prochazka L, Dong L, Andera L, Ralph SJ (2007) Tumour-initiating cells vs. cancer 'stem' cells and CD133: What's in the name? Biochem Biophys Res Commun 355:855-859. doi:10.1016/j.bbrc.2007. 01.159 (Pubitemid 46366906)
43. Hambardzumyan D, Squatrito M, Holland EC (2006) Radiation resistance and stem-like cells in brain tumors. Cancer Cell 10:454-456. doi:10.1016/j.ccr.2006. 11.008 (Pubitemid 44854752)
44. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A (2007) HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 17:165-172. doi:10.1016/j.cub.2006. 11.033 (Pubitemid 46107823)
45. Frank NY, Margaryan A, Huang Y, Schatton T, Waaga-Gasser AM, Gasser M, Sayegh MH, Sadee W, Frank MH (2005) ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 65:4320-4333. doi: 10.1158/0008-5472.CAN-04-3327 (Pubitemid 40775671)
46. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756-760. doi:10.1038/nature05236 (Pubitemid 44949604)
47. Mashour GA, Drissel SN, Frahm S, Farassati F, Martuza RL, Mautner VF, Kindler-Rohrborn A, Kurtz A (2005) Differential modulation of malignant peripheral nerve sheath tumor growth by omega-3 and omega-6 fatty acids. Oncogene 24:2367-2374 (Pubitemid 40546695)
48. ThomasSL, DeadwylerGD, TangJ, StubbsEBJr,MuirD,HiattKK, Clapp DW, De Vries GH (2006) Reconstitution of the NF1 GAP-related domain in NF1-deficient human Schwann cells. Biochem Biophys Res Commun 348:971-980. doi:S0006-291X(06)01704-910.1016/j.bbrc.2006.07.159 (Pubitemid 44233511)
49. Vogel KS, Klesse LJ, Velasco-Miguel S, Meyers K, Rushing EJ, Parada LF (1999) Mouse tumor model for neurofibromatosis type 1. Science 286:2176-2179
50. Bergeron JJ, Brenner MB, Thomas DY, Williams DB (1994) Calnexin: a membrane-bound chaperone of the endoplasmic reticulum. Trends Biochem Sci 19:124-128 (Pubitemid 24082790)
51. Kohno K, Normington K, Sambrook J, Gething MJ, Mori K (1993) The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol Cell Biol 13:877-890 (Pubitemid 23040253)
52. Ellgaard L, Ruddock LW (2005) The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep 6:28-32. doi:10.1038/sj.embor.7400311 (Pubitemid 41710070)
53. Cabibbo A, Pagani M, Fabbri M, Rocchi M, Farmery MR, Bul-leid NJ, Sitia R (2000) ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum. J Biol Chem 275:4827-4833 (Pubitemid 30108874)
54. Cox JS, Shamu CE, Walter P (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73:1197-1206 (Pubitemid 23180493)
55. Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274. doi:10.1038/16729 (Pubitemid 29051178)
56. Shi Y, Vattem KM, Sood R, An J, Liang J, Stramm L, Wek RC (1998) Identification and characterization of pancreatic eukary-otic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol 18:7499-7509 (Pubitemid 28533068)
57. Hancock CN, Macias A, Lee EK, Yu SY, Mackerell AD Jr, Shapiro P (2005) Identification of novel extracellular signal-regulated kinase docking domain inhibitors. J Med Chem 48:4586-4595. doi:10.1021/jm0501174 (Pubitemid 40993419)
58. Spyra M, Kluwe L, Hagel C, Nguyen R, Panse J, Kurtz A, Mautner VF, Rabkin SD, Demestre M (2011) Cancer stem cell-like cells derived from malignant peripheral nerve sheath tumors. PLoS ONE 6:e21099. doi:10.1371/journal.pone. 0021099
59. Farassati F, Pan W, Yamoutpour F, Henke S, Piedra M, Frahm S, Al-Tawil S, Mangrum WI, Parada LF, Rabkin SD, Martuza RL, Kurtz A (2008) Ras signaling influences permissiveness of malignant peripheral nerve sheath tumor cells to oncolytic herpes. Am J Pathol 173:1861-1872
60. Norman KL, Farassati F, Lee PW (2001) Oncolytic viruses and cancer therapy. Cytokine Growth Factor Rev 12:271-282 (Pubitemid 32588150)
61. Pan W, Bodempudi V, Esfandyari T, Farassati F (2009) Utilizing Ras signaling pathway to direct selective replication of herpes simplex virus-1. PLoS ONE 4:e6514
62. Tabu K, Kimura T, Sasai K, Wang L, Bizen N, Nishihara H, Taga T, Tanaka S (2010) Analysis of an alternative human CD133 promoter reveals the implication of Ras/ERK pathway in tumor stem-like hallmarks. Mol Cancer 9:39. doi:10.1186/1476-4598-9-39
63. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2:76-83. doi: 10.1038/35000025
64. Kato N, Shimmura S, Kawakita T, Miyashita H, Ogawa Y, Yoshida S, Higa K, Okano H, Tsubota K (2007) Beta-catenin activation and epithelial-mesenchymal transition in the patho-genesis ofpterygium. Invest Ophthalmol Vis Sci 48:1511-1517. doi:10.1167/iovs.06-1060 (Pubitemid 351261333)
65. Zheng G, Lyons JG, Tan TK, Wang Y, Hsu TT, Min D, Succar L, Rangan GK, Hu M, Henderson BR, Alexander SI, Harris DC (2009) Disruption of E-cadherin by matrix metalloproteinase directly mediates epithelial-mesenchymal transition downstream of transforming growth factor-beta1 in renal tubular epithelial cells. Am J Pathol 175:580-591. doi:10.2353/ajpath.2009.080983
66. McGuire JK, Li Q, Parks WC (2003) Matrilysin (matrix metalloproteinase-7) mediates E-cadherin ectodomain shedding in injured lung epithelium. Am J Pathol 162:1831-1843 (Pubitemid 36613042)
67. Monteiro J, Fodde R (2010) Cancer stemness and metastasis: therapeutic consequences and perspectives. Eur J Cancer 46: 1198-1203. doi:10.1016/j.ejca. 2010.02.030
68. Maheswaran S, Haber DA (2010) Circulating tumor cells: a window into cancer biology and metastasis. Curr Opin Genet Dev 20:96-99. doi:10.1016/j.gde.2009.12.002
69. Wang G, Yang ZQ, Zhang K (2010) Endoplasmic reticulum stress response in cancer: molecular mechanism and therapeutic potential. Am J Transl Res 2:65-74
70. Schleicher SM, Moretti L, Varki V, Lu B (2010) Progress in the unraveling of the endoplasmic reticulum stress/autophagy path-way and cancer: implications for future therapeutic approaches. Drug Resist Updates 13:79-86. doi:10.1016/j.drup.2010.04.002
71. Lisbona F, Hetz C (2009) Turning off the unfolded protein response: an interplay between the apoptosis machinery and ER stress signaling. Cell Cycle 8:1643-1644
72. Lisbona F, Rojas-Rivera D, Thielen P, Zamorano S, Todd D, Martinon F, Glavic A, Kress C, Lin JH, Walter P, Reed JC, Glimcher LH, Hetz C (2009) BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1alpha. Mol Cell 33: 679-691. doi:10.1016/j.molcel.2009.02.017