The Ras-like protein R-Ras2/TC21 is important for proper mammary gland development

Molecular Biology of the Cell

Volumn 23, Issue 12, 2012, Pages 2373-2387

  Larive, Romain M ^a,b   Abad, Antonio ^a,b   Cardaba, Clara M ^a,b   Hernańdez, Teresa ^a,b   Canãmero, Marta ^c   De Aĺava, Enrique ^a,b   Santos, Eugenio ^a,b   Alarcoń, Balbino ^d   Bustelo, Xosé R ^a,b  

^a Centro de Investigacion del Cancer   (Spain)

^b Salamanca Spain   (Spain)

^c Structural Biology and Biocomputing Programme   (Spain)

^d CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; PROTEIN KINASE B; PROTEIN R RAS2 TC21; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST DEVELOPMENT; BREAST EPITHELIUM; CARDIOVASCULAR PARAMETERS; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; FEMALE; FERTILITY; GENETIC REGULATION; GROWTH RATE; HUMAN; HUMAN TISSUE; IN VIVO STUDY; KNOCKOUT MOUSE; MAMMARY GLAND; MORPHOGENESIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PUBERTY;

ANIMALS; BETA-GALACTOSIDASE; BLOTTING, WESTERN; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; EMBRYO, MAMMALIAN; EPITHELIAL CELLS; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MAMMARY GLANDS, ANIMAL; MEMBRANE PROTEINS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOMERIC GTP-BINDING PROTEINS; PROMOTER REGIONS, GENETIC; RAS PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84862544795     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-01-0060     Document Type: Article

References (52)

1. Arora S, Matta A, Shukla NK, Deo SV, Ralhan R (2005). Identification of differentially expressed genes in oral squamous cell carcinoma. Mol Carcinog 42, 97-108.
2. Barker KT, Crompton MR (1998). Ras-related TC21 is activated by mutation in a breast cancer cell line, but infrequently in breast carcinomas in vivo. Br J Cancer 78, 296-300. (Pubitemid 28336414)
3. Calvo F, Crespo P (2009). Structural and spatial determinants regulating TC21 activation by RasGRF family nucleotide exchange factors. Mol Biol Cell 20, 4289-4302.
4. Castro-Castro A, Ojeda V, Barreira M, Sauzeau V, Navarro-Lerida I, Muriel O, Couceiro JR, Pimentel-Muinos FX, Del Pozo MA, Bustelo XR (2011). Coronin 1A promotes a cytoskeletal-based feedback loop that facilitates Rac1 translocation and activation. EMBO J 30, 3913-3927.
5. Chan AM, Miki T, Meyers KA, Aaronson SA (1994). A human oncogene of the RAS superfamily unmasked by expression cDNA cloning. Proc Natl Acad Sci USA 91, 7558-7562. (Pubitemid 24238224)
6. Clark GJ, Kinch MS, Gilmer TM, Burridge K, Der CJ (1996). Overexpression of the Ras-related TC21/R-Ras2 protein may contribute to the development of human breast cancers. Oncogene 12, 169-176.
7. Colicelli J (2004). Human RAS superfamily proteins and related GTPases. Sci STKE 2004, RE13.
8. Daniel CW, De Ome KB, Young JT, Blair PB, Faulkin LJ Jr (1968). The in vivo life span of normal and preneoplastic mouse mammary glands: a serial transplantation study. Proc Natl Acad Sci USA 61, 53-60.
9. Delgado P, Cubelos B, Calleja E, Martinez-Martin N, Cipres A, Merida I, Bellas C, Bustelo XR, Alarcon B (2009). Essential function for the GTPase TC21 in homeostatic antigen receptor signaling. Nat Immunol 10, 880-888.
10. Deome KB, Faulkin LJ Jr, Bern HA, Blair PB (1959). Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res 19, 515-520.
11. Drivas GT, Shih A, Coutavas E, Rush MG, D'Eustachio P (1990). Characterization of four novel ras-like genes expressed in a human teratocarcinoma cell line. Mol Cell Biol 10, 1793-1798.
12. Drosten M, Dhawahir A, Sum EY, Urosevic J, Lechuga CG, Esteban LM, Castellano E, Guerra C, Santos E, Barbacid M (2010). Genetic analysis of Ras signalling pathways in cell proliferation, migration and survival. EMBO J 29, 1091-1104.
13. Esteban LM et al. (2001). 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. (Pubitemid 32156364)
14. Gjorevski N, Nelson CM (2011). Integrated morphodynamic signalling of the mammary gland. Nat Rev 12, 581-593.
15. Graham SM, Cox AD, Drivas G, Rush MG, D'Eustachio P, Der CJ (1994). Aberrant function of the Ras-related protein TC21/R-Ras2 triggers malignant transformation. Mol Cell Biol 14, 4108-4115. (Pubitemid 24160816)
16. Graham SM, Oldham SM, Martin CB, Drugan JK, Zohn IE, Campbell S, Der CJ (1999). TC21 and Ras share indistinguishable transforming and differentiating activities. Oncogene 18, 2107-2116. (Pubitemid 29178579)
17. Graham SM, Vojtek AB, Huff SY, Cox AD, Clark GJ, Cooper JA, Der CJ (1996). TC21 causes transformation by Raf-independent signaling pathways. Mol Cell Biol 16, 6132-6140. (Pubitemid 26360973)
18. Huang Y, Rangwala F, Fulkerson PC, Ling B, Reed E, Cox AD, Kamholz J, Ratner N (2004). Role of TC21/R-Ras2 in enhanced migration of neurofibromin-deficient Schwann cells. Oncogene 23, 368-378. (Pubitemid 38174990)
19. Huang Y, Saez R, Chao L, Santos E, Aaronson SA, Chan AM (1995). A novel insertional mutation in the TC21 gene activates its transforming activity in a human leiomyosarcoma cell line. Oncogene 11, 1255-1260.
20. Keely PJ, Rusyn EV, Cox AD, Parise LV (1999). R-Ras signals through specific integrin alpha cytoplasmic domains to promote migration and invasion of breast epithelial cells. J Cell Biol 145, 1077-1088. (Pubitemid 29270064)
21. Kelley GG, Reks SE, Smrcka AV (2004). Hormonal regulation of phospholipase Cepsilon through distinct and overlapping pathways involving G12 and Ras family G-proteins. Biochem J 378, 129-139. (Pubitemid 38299550)
22. Komatsu M, Ruoslahti E (2005). R-Ras is a global regulator of vascular regeneration that suppresses intimal hyperplasia and tumor angiogenesis. Nat Med 11, 1346-1350. (Pubitemid 41752916)
23. Kozian DH, Augustin HG (1997). Transcriptional regulation of the Ras-related protein TC21/R-Ras2 in endothelial cells. FEBS Lett 414, 239-242. (Pubitemid 27389370)
24. Larkin JE, Frank BC, Gaspard RM, Duka I, Gavras H, Quackenbush J (2004). Cardiac transcriptional response to acute and chronic angiotensin II treatments. Physiol Genomics 18, 152-166. (Pubitemid 39319497)
25. Lee JH et al. (2011). Greater expression of TC21/R-ras2 in highly aggressive malignant skin cancer. Int J Dermatol 50, 956-960.
26. Light Y, Paterson H, Marais R (2002). 14-3-3 antagonizes Ras-mediated Raf-1 recruitment to the plasma membrane to maintain signaling fidelity. Mol Cell Biol 22, 4984-4996. (Pubitemid 34700691)
27. Lopez-Barahona M, Bustelo XR, Barbacid M (1996). The TC21 oncoprotein interacts with the Ral guanosine nucleotide dissociation factor. Oncogene 12, 463-470. (Pubitemid 26059639)
28. Luo H, Hao X, Ge C, Zhao F, Zhu M, Chen T, Yao M, He X, Li J (2010). TC21 promotes cell motility and metastasis by regulating the expression of E-cadherin and N-cadherin in hepatocellular carcinoma. Int J Oncol 37, 853-859.
29. Macha MA, Matta A, Sriram U, Thakkar A, Shukla NK, Datta Gupta S, Ralhan R (2009). Clinical significance of TC21 overexpression in oral cancer. J Oral Pathol Med 39, 477-485.
30. Martinez-Martin N et al. (2011). T cell receptor internalization from the immunological synapse is mediated by TC21 and RhoG GTPase-dependent phagocytosis. Immunity 35, 208-222.
31. McFall A, Ulku A, Lambert QT, Kusa A, Rogers-Graham K, Der CJ (2001). Oncogenic Ras blocks anoikis by activation of a novel effector pathway independent of phosphatidylinositol 3-kinase. Mol Cell Biol 21, 5488-5499. (Pubitemid 32702453)
32. Mendes-Pereira AM et al. (2012). Genome-wide functional screen identifies a compendium of genes affecting sensitivity to tamoxifen. Proc Natl Acad Sci USA 109, 2730-2735.
33. Movilla N, Crespo P, Bustelo XR (1999). Signal transduction elements of TC21, an oncogenic member of the R-Ras subfamily of GTP-binding proteins. Oncogene 18, 5860-5869. (Pubitemid 29520442)
34. Murphy GA, Graham SM, Morita S, Reks SE, Rogers-Graham K, Vojtek A, Kelley GG, Der CJ (2002). Involvement of phosphatidylinositol 3-kinase, but not RalGDS, in TC21/R-Ras2-mediated transformation. J Biol Chem 277, 9966-9975. (Pubitemid 34968104)
35. Nagi A, Gertsenstein M, Vintersen K, Behringer K (2003). Manipulating the Mouse Embryo: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Press.
36. Nunez Rodriguez N, Lee IN, Banno A, Qiao HF, Qiao RF, Yao Z, Hoang T, Kimmelman AC, Chan AM (2006). Characterization of R-ras3/m-ras null mice reveals a potential role in trophic factor signaling. Mol Cell Biol 26, 7145-7154. (Pubitemid 44477691)
37. Ohba Y, Mochizuki N, Yamashita S, Chan AM, Schrader JW, Hattori S, Nagashima K, Matsuda M (2000). Regulatory proteins of R-Ras, TC21/R-Ras2, and M-Ras/R-Ras3. J Biol Chem 275, 20020-20026. (Pubitemid 30441610)
38. Rokavec M, Schroth W, Amaral SM, Fritz P, Antoniadou L, Glavac D, Simon W, Schwab M, Eichelbaum M, Brauch H (2008). A polymorphism in the TC21 promoter associates with an unfavorable tamoxifen treatment outcome in breast cancer. Cancer Res 68, 9799-9808.
39. Rong R, He Q, Liu Y, Sheikh MS, Huang Y (2002). TC21 mediates transformation and cell survival via activation of phosphatidylinositol 3-kinase/Akt and NF-kappaB signaling pathway. Oncogene 21, 1062-1070. (Pubitemid 34174518)
40. Rosario M, Paterson HF, Marshall CJ (1999). Activation of the Raf/MAP kinase cascade by the Ras-related protein TC21 is required for the TC21-mediated transformation of NIH 3T3 cells. EMBO J 18, 1270-1279. (Pubitemid 29110311)
41. Rosario M, Paterson HF, Marshall CJ (2001). Activation of the Ral and phosphatidylinositol 3' kinase signaling pathways by the ras-related protein TC21. Mol Cell Biol 21, 3750-3762. (Pubitemid 32466988)
42. Sauzeau V, Jerkic M, Lopez-Novoa JM, Bustelo XR (2007). Loss of Vav2 proto-oncogene causes tachycardia and cardiovascular disease in mice. Mol Biol Cell 18, 943-952. (Pubitemid 46399499)
43. Sauzeau V, Sevilla MA, Rivas-Elena JV, de Alava E, Montero MJ, Lopez-Novoa JM, Bustelo XR (2006). Vav3 proto-oncogene deficiency leads to sympathetic hyperactivity and cardiovascular dysfunction. Nat Med 12, 841-845. (Pubitemid 44050076)
44. Shang X et al. (2011). R-Ras and Rac GTPase cross-talk regulates hematopoietic progenitor cell migration, homing, and mobilization. J Biol Chem 286, 24068-24078.
45. Singh G et al. (2012). R-Ras is required for murine dendritic cell maturation and CD4+ T-cell priming. Blood 119, 1693-1701.
46. Sleeman KE, Kendrick H, Ashworth A, Isacke CM, Smalley MJ (2006). CD24 staining of mouse mammary gland cells defines luminal epithelial, myoepithelial/basal and non-epithelial cells. Breast Cancer Res 8, R7.
47. Sternlicht MD, Kouros-Mehr H, Lu P, Werb Z (2006). Hormonal and local control of mammary branching morphogenesis. Differentiation 74, 365-381. (Pubitemid 44215408)
48. Sternlicht MD, Sunnarborg SW, Kouros-Mehr H, Yu Y, Lee DC, Werb Z (2005). Mammary ductal morphogenesis requires paracrine activation of stromal EGFR via ADAM17-dependent shedding of epithelial amphiregulin. Development 132, 3923-3933. (Pubitemid 41410256)
49. Stingl J, Raouf A, Eirew P, Eaves CJ (2006). Deciphering the mammary epithelial cell hierarchy. Cell Cycle 5, 1519-1522. (Pubitemid 44091971)
50. Theiler K (1989). The House Mouse: Atlas of Embryonic Development, New York: Springer-Verlag.
51. Welm BE, Dijkgraaf GJ, Bledau AS, Welm AL, Werb Z (2008). Lentiviral transduction of mammary stem cells for analysis of gene function during development and cancer. Cell Stem Cell 2, 90-102.
52. Zhu Y, Zhong X, Zheng S, Ge Z, Du Q, Zhang S (2005). Transformation of immortalized colorectal crypt cells by microcystin involving constitutive activation of Akt and MAPK cascade. Carcinogenesis 26, 1207-1214. (Pubitemid 41417897)