Isoform-specific ras functions in development and cancer

Future Oncology

Volumn 5, Issue 1, 2009, Pages 105-116

  Quinlan, Margaret ^a   Settleman, Jeffrey ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cancer; Development; GTPases; Ras; Stem cells

Indexed keywords

GUANOSINE TRIPHOSPHATE; K RAS PROTEIN; RAS PROTEIN; ISOPROTEIN;

CARCINOGENESIS; CELL SURFACE; CELLULAR DISTRIBUTION; DEVELOPMENT; DEVELOPMENTAL DISORDER; EMBRYONIC STEM CELL; GENE MUTATION; GERM LINE; HUMAN; HYDROLYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; GENETICS; METABOLISM; NEOPLASM; PHYSIOLOGY;

HUMANS; NEOPLASMS; PROTEIN ISOFORMS; RAS PROTEINS; SIGNAL TRANSDUCTION;

EID: 65349150639     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/14796694.5.1.105     Document Type: Review

References (81)

1. Giehl K: Oncogenic Ras in tumour progression and metastasis. Biol. Chem. 386, 193-205 (2005).
2. Malumbres M, Barbacid M: RAS oncogenes: the first 30 years. Nat. Rev. Cancer 3, 459-465 (2003).
3. Rajalingam K, Schreck R, Rapp UR, Albert S: Ras oncogenes and their downstream targets. Biochim. Biophys. Acta 1773, 1177-1195 (2007).
4. Adjei AA: Blocking oncogenic Ras signaling for cancer therapy. J. Natl Cancer Inst. 93, 1062-1074 (2001).
5. Downward J: Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3, 11-22 (2003).
6. Drivas GT, Palmieri S, D'Eustachio P, Rush MG: Evolutionary grouping of the RAS-protein family. Biochem. Biophys. Res. Commun. 176, 1130-1135 (1991).
7. Jekely G: Small GTPases and the evolution of the eukaryotic cell. Bioessays 25, 1129-1138 (2003).
8. Jiang SY, Ramachandran S: Comparative and evolutionary analysis of genes encoding small GTPases and their activating-proteins in eukaryotic genomes. Physiol. Genomics 24, 235-251 (2006).
9. Colicelli J: Human RAS superfamily proteins and related GTPases. Sci. STKE 250, RE13 (2004).
10. Crespo P, Leon J: Ras proteins in the control of the cell cycle and cell differentiation. Cell. Mol. Life Sci. 57, 1613-1636 (2000).
11. Friday BB, Adjei AA: K-ras as a target for cancer therapy. Biochim. Biophys. Acta 1756, 127-144 (2005).
12. Herrmann C: Ras-effector interactions: after one decade. Curr. Opin. Struct. Biol. 13, 122-129 (2003).
13. Campbell PM, Singh A, Williams FJ et al.: Genetic and pharmacologic dissection of ras effector utilization in oncogenesis. Meth. Enzymol. 407, 195-217 (2005).
14. Rodriguez-Viciana P, Tetsu O, Oda K, Okada J, Rauen K, McCormick F: Cancer targets in the Ras pathway. Cold Spring Harb. Symp. Quant. Biol. 70, 461-467 (2005).
15. Rapp UR, Goldsborough MD, Mark GE et al.: Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus. Proc. Natl Acad. Sci. USA 80, 4218-4222 (1983).
16. McCubrey JA, Steelman LS, Chappell WH et al.: Roles of the Raf/ MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim. Biophys. Acta 1773, 1263-1284 (2007).
17. Ellis CA, Clark G: The importance of being K-Ras. Cell. Signal. 12, 425-434 (2000).
18. Gorfe AA., Grant BJ, McCammon JA: Mapping the nucleotide and isoform dependent structural and dynamical features of Ras proteins. Structure 16, 885-896 (2008).
19. Hancock JF: Ras proteins: different signals from different locations. Nat. Rev. Mol. Cell Biol. 4, 373-384 (2003).
20. Laude AJ, Prior IA: Palmitoylation and localisation of RAS isoforms are modulated by the hypervariable linker domain. J. Cell Sci. 121, 421-427 (2008).
21. Plowman SJ, Hancock JF: Ras signaling from plasma membrane and endomembrane microdomains. Biochim. Biophys. Acta 1746, 274-283 (2005).
22. Hancock JF, Parton RG: Ras plasma membrane signalling platforms. Biochem. J. 389, 1-11 (2005).
23. Parton RG, Hancock JF: Lipid rafts and plasma membrane microorganization: insights from Ras. Trends Cell Biol. 14, 141-147 (2004).
24. Mor A, Philips MR: Compartmentalized Ras/MAPK signaling. Annu. Rev. Immunol. 24, 771-800 (2006).
25. Wright LP, Philips MR: Thematic review series: lipid posttranslational modifications. CAAX modification and membrane targeting of Ras. J. Lipid Res. 47, 883-891 (2006).
26. Quatela SE, Philips MR: Ras signaling on the Golgi. Curr. Opin. Cell Biol. 18, 162-167 (2006).
27. Philips MR: Compartmentalized signalling of Ras. Biochem. Soc. Trans. 33, 657-661 (2005).
28. Jura N, Bar-Sagi D: Mapping cellular routes of Ras: a ubiquitin trail. Cell Cycle 5, 2744-2747 (2006).
29. Roberts ML, Drosopoulos KG, Vasileiou I et al.: Microarray analysis of the differential transformation mediated by Kirsten and Harvey Ras oncogenes in a human colorectal adenocarcinoma cell line. Int. J. Cancer 118, 616-627 (2006).
30. Zuber J, Tchernitsa OI, Hinzmann B et al.: A genome-wide survey of RAS transformation targets. Nat. Genet. 24, 144-152 (2000).
31. Michaelson D, Ali W, Chiu VK et al.: Postprenylation CAAX processing is required for proper localization of Ras but not Rho GTPases. Mol. Biol. Cell 16, 1606-1616 (2005).
32. Apolloni A, Prior IA, Lindsay M, Parton RG, Hancock JF: H-ras but not K-ras traffics to the plasma membrane through the exocytic pathway. Mol. Cell Biol. 20, 2475-2487 (2000).
33. Choy E, Chiu VK, Sillerti J et al.: Endomembrane trafficking of ras: the CAAK motif targets proteins to the ER and Golgi. Cell 98, 69-80 (1999).
34. Choy E, Philips M: Green fluorescent protein-tagged Ras proteins for intracellular localization. Meth. Enzymol. 332, 50-64 (2001).
35. Gomez GA, Daniotti JL: H-Ras dynamically interacts with recycling endosomes in CHO-K1 cells: involvement of Rab5 and Rab11 in the trafficking of H-Ras to this pericentriolar endocytic compartment. J. Biol. Chem. 280, 34997-35010 (2005).
36. Goodwin JS, Drake KR, Remmert CL, Kenworthy AK: Ras diffusion is sensitive to plasma membrane viscosity. Biophys. J. 89, 1398-1410 (2005).
37. Rocks O, Peyker A, Kabms M et al.: An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307, 1746-1752 (2005).
38. Rotblat B, Yizhar O, Haklai R, Ashery U, Kloog Y: Ras and its signals diffuse through the cell on randomly moving nanoparticles. Cancer Res. 66, 1974-1981 (2006).
39. Thissen JA, Gross JM, Subramanian K, Meyer T, Casey PJ: Prenylation-dependent association of Ki-Ras with microtubules. Evidence for a role in subcellular trafficking. J. Biol. Chem. 272, 30362-30370 (1997).
40. Bivona TG, Quatela SE, Bodemann BO et al.: PKC regulates a farnesyl-electrostatic switch on K-Ras that promotes its association with Bcl-XL on mitochondria and induces apoptosis. Mol. Cell 21, 481-493 (2006).
41. 2+/calmodulin. J. Cell Biol. 170, 429-441 (2005).
42. Prior IA, Harding A, Yan J, Sluimer J, Parton RG, Hancock JF: GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat. Cell Biol. 3, 368-375 (2001).
43. Berthiaume LG: Insider information: how palmitoylation of Ras makes it a signaling double agent. Sci. STKE 152, PE41 (2002).
44. Jura N, Scotto-Lavino E, Sobczyk A, Bar-Sagi D: Differential modification of Ras proteins by ubiquitination. Mol. Cell 21, 679-687 (2006).
45. Traverse S, Gomez N, Paterson H, Marshall C, Cohen P: Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J. 288(Pt 2), 351-355 (1992).
46. Esteban LM, Vicario-Abejon C, Fernandez-Salguero P et al.: Targeted genomic disruption of H-ras and N-ras, individually or in combination, reveals the dispensability of both loci for mouse growth and development. Mol. Cell. Biol. 21, 1444-1452 (2001).
47. Johnson L, Greenbaum D, Cichowski K et al.: K-ras is an essential gene in the mouse with partial functional overlap with N-ras. Genes Dev. 11, 2468-2481 (1997).
48. Koera K, Nakamura K, Nakao K et al.: K-ras is essential for the development of the mouse embryo. Oncogene 15, 1151-1159 (1997).
49. Umanoff H, Edelmann W, Pellicer A, Kucherlapati R: The murine N-ras gene is not essential for growth and development. Proc. Natl Acad. Sci. USA 92, 1709-1713 (1995).
50. Aoki Y, Niihori T, Kawame H et al.: Germline mutations in HRAS proto-oncogene cause Costello syndrome. Nat. Genet. 37, 1038-1040 (2005).
51. Aoki Y, Niihori T, Narumi Y, Kure S, Matsubara Y: The RAS/MAPK syndromes: novel roles of the RAS pathway in human genetic disorders. Hum. Mutat. 29(8), 992-1006 (2008).
52. Bentires-Alj M, Kontaridis MI, Neel BG: Stops along the RAS pathway in human genetic disease. Nat. Med. 12, 283-285 (2006).
53. Kerr B, Delrue MA, Sigaudy S et al.: Genotype-phenotype correlation in Costello syndrome: HRAS mutation analysis in 43 cases. J. Med. Genet. 43, 401-405 (2006).
54. Kratz CP, Schubbert S, Bollag G, Niemeyer CM, Shannon KM, Zenker M: Germline mutations in components of the Ras signaling pathway in Noonan syndrome and related disorders. Cell Cycle 5, 1607-1611 (2006).
55. Lee JS, Tartaglia M, Gelb BD et al.: Phenotypic and genotypic characterisation of Noonan-like/multiple giant cell lesion syndrome. J. Med. Genet. 42, e11 (2005).
56. Niihori T, Aoki Y, Narumi Y et al.: Germline KRAS and BRAF mutations in cardio-facio-cutaneous syndrome. Nat. Genet. 38, 294-296 (2006).
57. Roberts A, Allanson J, Jadico SK et al.: The cardiofaciocutaneous syndrome. J. Med. Genet. 43, 833-842 (2006).
58. Rodriguez-Viciana P, Tetsu O, Tidyman WE et al.: Germline mutations in genes within the MAPK pathway cause cardio-facio-cutaneous syndrome. Science 311, 1287-1290, (2006).
59. Schubbert S, Zenker M, Rowe SL et al.: Germline KRAS mutations cause Noonan syndrome. Nat. Genet. 38, 331-336 (2006).
60. Tartaglia M, Gelb BD: Noonan syndrome and related disorders: genetics and pathogenesis. Annu. Rev. Genomics Hum. Genet. 6, 45-68 (2005).
61. Katsuki M, Kimura M, Hata J et al.: Embryonal tumors from transgenic mouse zygotes carrying human activated c-Ha-ras genes. Mol. Biol. Med. 6, 567-572 (1989).
62. Schuhmacher AJ, Guerra C, Sauzeau V, Canamero M, Bustelo XR, Barbacid M: A mouse model for Costello syndrome reveals an Ang II-mediated hypertensive condition. J. Clin. Invest. 118, 2169-2179 (2008).
63. Oliveira JB, Bidere N, Niemela JE et al.: NRAS mutation causes a human autoimmune lymphoproliferative syndrome. Proc. Natl Acad. Sci. USA 104, 8953-8958 (2007).
64. Bar-Sagi D, Feramisco JR: Microinjection of the ras oncogene protein into PC12 cells induces morphological differentiation. Cell 42, 841-848 (1985).
65. Benito M, Porras A, Nebreda AR, Santos E: Differentiation of 3T3-L1 fibroblasts to adipocytes induced by transfection of ras oncogenes. Science 253, 565-568 (1991).
66. Qui MS, Green SH: PC12 cell neuronal differentiation is associated with prolonged p21ras activity and consequent prolonged ERK activity. Neuron 9, 705-717 (1992).
67. Schulz WA: Understanding urothelial carcinoma through cancer pathways. Int. J. Cancer 119, 1513-1518 (2006).
68. Yon J, Robinson RA: ras gene mutations in salivary gland tumors. Arch. Pathol. Lab. Med. 124, 836-839 (2000).
69. Bauer J, Curtin JA, Pinkel D, Bastian BC: Congenital melanocytic nevi frequently harbor NRAS mutations but no BRAF mutations. J. Invest. Dermatol. (2006).
70. Ganguly S, Murty VV, Samardego F, Reuter VE, Bosl GJ, Chaganti RS: Detection of preferential NRAS mutations in human male germ cell tumors by the polymerase chain reaction. Genes Chromosomes Cancer 1, 228-232 (1990).
71. Parikh C, Subrahmanyam R, Ren R: Oncogenic NRAS rapidly and efficiently induces CMML- and AML-like diseases in mice. Blood 108, 2349-2357 (2006).
72. Quinlan MP, Quatela SE, Philips MR, Settleman J: Activated Kras, but not Hras or Nras, may initiate tumors of endodermal origin via stem cell expansion. Mol. Cell. Biol. 28(8), 2659-2674 (2008).
73. Quinlan MP, Settleman J: Explaining the preponderance of Kras mutations in human cancer: an isoform-specific function in stem cell expansion. Cell Cycle 7, 1332-1335 (2008).
74. Quinlan MP: The Ad5 12S growth factor induces F9 cell proliferation and differentiation. Oncogene 4, 1051-1055 (1989).
75. Verheijen MH, Wolthuis RM, Bos JL, Defize LH: The Ras/Erk pathway induces primitive endoderm but prevents parietal endoderm differentiation of F9 embryonal carcinoma cells. J. Biol. Chem. 274, 1487-1494 (1999).
76. Yamaguchi-Iwai Y, Satake M, Murakami Y, Sakai M, Muramatsu M, Ito Y: Differentiation of F9 embryonal carcinoma cells induced by the c-jun and activated c-Ha-ras oncogenes. Proc. Natl Acad. Sci. USA 87, 8670-8674 (1990).
77. Kim CF, Jackson EL, Woolfenden AE et al.: Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121, 823-835 (2005).
78. Haigis KM, Kendall KR, Wang Y et al.: Differential effects of oncogenic K-Ras and N-Ras on proliferation, differentiation and tumor progression in the colon. Nat. Genet. 40, 600-608 (2008).
79. Luo F, Hamoudi R, Brooks DG, Patek CE, Arends MJ: Stem cell gene expression changes induced specifically by mutated K-ras. Gene Expr. 14, 101-115 (2007).
80. Takahashi K, Mitsui K, Yamanaka S: Role of ERas in promoting tumour-like properties in mouse embryonic stem cells. Nature 423, 541-545 (2003).
81. Guo X, Stratton L, Schrader JW: Expression of activated M-Ras in hemopoietic stem cells initiates leukemogenic transformation, immortalization and preferential generation of mast cells. Oncogene 25, 4241-4244 (2006).