Rab31 expression levels modulate tumor-relevant characteristics of breast cancer cells

Molecular Cancer

Volumn 11, Issue , 2012, Pages

  Grismayer, Bettina ^a   Sölch, Susanne ^a   Seubert, Bastian ^a   Kirchner, Thomas ^b   Schäfer, Sonja ^a   Baretton, Gustavo ^c   Schmitt, Manfred ^a   Luther, Thomas ^b,c   Krüger, Achim ^a   Kotzsch, Matthias ^c   Magdolen, Viktor ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b Medizinisches Labor Ostsachsen   (Germany)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Adhesion; Breast cancer; GTP binding protein; Intracellular vesicle transport; Invasion; Proliferation; rab31; Tumor cell phenotype

Indexed keywords

MATRIGEL; RAB PROTEIN; RAB31 PROTEIN; SCLEROPROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CELL ADHESION; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PLASMID; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TUMOR XENOGRAFT; WESTERN BLOTTING;

ANIMALS; ANTIBODIES; BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, NUDE; RAB GTP-BINDING PROTEINS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84865281929     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-11-62     Document Type: Article

References (56)

1. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009, 10:513-525.
2. Goud B, Gleeson PA. TGN golgins, Rabs and cytoskeleton: regulating the Golgi trafficking highways. Trends Cell Biol 2010, 20:329-336. 10.1016/j.tcb.2010.02.006, 20227882.
3. Barr FA. Rab GTPase function in Golgi trafficking. Semin Cell Dev Biol 2009, 20:780-783. 10.1016/j.semcdb.2009.03.007, 19508857.
4. Rodriguez-Gabin AG, Cammer M, Almazan G, Charron M, Larocca JN. Role of rRAB22b, an oligodendrocyte protein, in regulation of transport of vesicles from trans Golgi to endocytic compartments. J Neurosci Res 2001, 66:1149-1160. 10.1002/jnr.1253, 11746448.
5. Ng EL, Wang Y, Tang BL. Rab22B's role in trans-Golgi network membrane dynamics. Biochem Biophys Res Commun 2007, 361:751-757. 10.1016/j.bbrc.2007.07.076, 17678623.
6. Rodriguez-Gabin AG, Yin X, Si Q, Larocca JN. Transport of mannose-6-phosphate receptors from the trans-Golgi network to endosomes requires Rab31. Exp Cell Res 2009, 315:2215-2230. 10.1016/j.yexcr.2009.03.020, 2753287, 19345684.
7. Ng EL, Ng JJ, Liang F, Tang BL. Rab22B is expressed in the CNS astroglia lineage and plays a role in epidermal growth factor receptor trafficking in A431 cells. J Cell Physiol 2009, 221:716-728. 10.1002/jcp.21911, 19725050.
8. Lodhi IJ, Chiang SH, Chang L, Vollenweider D, Watson RT, Inoue M, Pessin JE, Saltiel AR. Gapex-5, a Rab31 guanine nucleotide exchange factor that regulates Glut4 trafficking in adipocytes. Cell Metab 2007, 5:59-72. 10.1016/j.cmet.2006.12.006, 1779820, 17189207.
9. Kajiho H, Sakurai K, Minoda T, Yoshikawa M, Nakagawa S, Fukushima S, Kontani K, Katada T. Characterization of RIN3 as a guanine nucleotide exchange factor for the Rab5 subfamily GTPase Rab31. J Biol Chem 2011, 286:24364-24373. 10.1074/jbc.M110.172445, 3129215, 21586568.
10. Heinonen M, Hemmes A, Salmenkivi K, Abdelmohsen K, Vilen ST, Laakso M, Leidenius M, Salo T, Hautaniemi S, Gorospe M, Heikkila P, Haglund C, Ristimaki A. Role of RNA binding protein HuR in ductal carcinoma in situ of the breast. J Pathol 2011, 224:529-539. 10.1002/path.2889, 21480233.
11. Rodriguez-Gabin AG, Ortiz E, Demoliner K, Si Q, Almazan G, Larocca JN. Interaction of Rab31 and OCRL-1 in oligodendrocytes: its role in transport of mannose 6-phosphate receptors. J Neurosci Res 2010, 88:589-604. 3133691, 19795375.
12. Chia WJ, Tang BL. Emerging roles for Rab family GTPases in human cancer. Biochim Biophys Acta 2009, 1795:110-116.
13. Caswell PT, Spence HJ, Parsons M, White DP, Clark K, Cheng KW, Mills GB, Humphries MJ, Messent AJ, Anderson KI, McCaffrey MW, Ozanne BW, Norman JC. Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments. Dev Cell 2007, 13:496-510. 10.1016/j.devcel.2007.08.012, 17925226.
14. Abba MC, Hu Y, Sun H, Drake JA, Gaddis S, Baggerly K, Sahin A, Aldaz CM. Gene expression signature of estrogen receptor alpha status in breast cancer. BMC Genomics 2005, 6:37. 10.1186/1471-2164-6-37, 555753, 15762987.
15. Kotzsch M, Sieuwerts AM, Grosser M, Meye A, Fuessel S, Meijer-van Gelder ME, Smid M, Schmitt M, Baretton G, Luther T, Magdolen V, Foekens JA. Urokinase receptor splice variant uPAR-del4/5-associated gene expression in breast cancer: identification of rab31 as an independent prognostic factor. Breast Cancer Res Treat 2008, 111:229-240. 10.1007/s10549-007-9782-6, 17952591.
16. Subramani D, Alahari SK. Integrin-mediated function of Rab GTPases in cancer progression. Mol Cancer 2010, 9:312. 10.1186/1476-4598-9-312, 3003658, 21143914.
17. Cheng KW, Lahad JP, Gray JW, Mills GB. Emerging role of RAB GTPases in cancer and human disease. Cancer Res 2005, 65:2516-2519. 10.1158/0008-5472.CAN-05-0573, 15805241.
18. Cheng JM, Volk L, Janaki DK, Vyakaranam S, Ran S, Rao KA. Tumor suppressor function of Rab25 in triple-negative breast cancer. Int J Cancer 2010, 126:2799-2812.
19. Seiz L, Kotzsch M, Grebenchtchikov NI, Geurts-Moespot AJ, Fuessel S, Goettig P, Gkazepis A, Wirth MP, Schmitt M, Lossnitzer A, Sweep FC, Magdolen V. Polyclonal antibodies against kallikrein-related peptidase 4 (KLK4): immunohistochemical assessment of KLK4 expression in healthy tissues and prostate cancer. Biol Chem 2010, 391:391-401.
20. Goody RS, Rak A, Alexandrov K. The structural and mechanistic basis for recycling of Rab proteins between membrane compartments. Cell Mol Life Sci 2005, 62:1657-1670. 10.1007/s00018-005-4486-8, 15924270.
21. Luther T, Kotzsch M, Meye A, Langerholc T, Fussel S, Olbricht N, Albrecht S, Ockert D, Muehlenweg B, Friedrich K, Grosser M, Schmitt M, Baretton G, Magdolen V. Identification of a novel urokinase receptor splice variant and its prognostic relevance in breast cancer. Thromb Haemost 2003, 89:705-717.
22. Sato S, Kopitz C, Grismayer B, Beaufort N, Reuning U, Schmitt M, Luther T, Kotzsch M, Krüger A, Magdolen V. Overexpression of the urokinase receptor mRNA splice variant uPAR-del4/5 affects tumor-associated processes of breast cancer cells in vitro and in vivo. Breast Cancer Res Treat 2010, 127:649-657.
23. Chambers AF. MDA-MB-435 and M14 cell lines: identical but not M14 melanoma?. Cancer Res 2009, 69:5292-5293. 10.1158/0008-5472.CAN-09-1528, 19549886.
24. Agola J, Jim P, Ward H, Basuray S, Wandinger-Ness A. Rab GTPases as regulators of endocytosis, targets of disease and therapeutic opportunities. Clin Genet 2012,
25. Yang PS, Yin PH, Tseng LM, Yang CH, Hsu CY, Lee MY, Horng CF, Chi CW. Rab5A is associated with axillary lymph node metastasis in breast cancer patients. Cancer Sci 2011, 102:2172-2178. 10.1111/j.1349-7006.2011.02089.x, 21895870.
26. Hendrix A, Braems G, Bracke M, Seabra M, Gahl W, De Wever O, Westbroek W. The secretory small GTPase Rab27B as a marker for breast cancer progression. Oncotarget 2010, 1:304-308. 3058367,3058367, 21304180.
27. Chen D, Guo J, Miki T, Tachibana M, Gahl WA. Molecular cloning of two novel rab genes from human melanocytes. Gene 1996, 174:129-134. 10.1016/0378-1119(96)00509-4, 8863739.
28. Yim EK, Tong SY, Ho EM, Bae JH, Um SJ, Park JS. Anticancer effects on TACC3 by treatment of paclitaxel in HPV-18 positive cervical carcinoma cells. Oncol Rep 2009, 21:549-557.
29. Kotzsch M, Dorn J, Doetzer K, Schmalfeldt B, Krol J, Baretton G, Kiechle M, Schmitt M, Magdolen V. mRNA expression levels of the biological factors uPAR, uPAR-del4/5, and rab31, displaying prognostic value in breast cancer, are not clinically relevant in advanced ovarian cancer. Biol Chem 2011, 392:1047-1051.
30. Hwang KA, Park SH, Yi BR, Choi KC. Gene alterations of ovarian cancer cells expressing estrogen receptors by estrogen and bisphenol a using microarray analysis. Lab Anim Res 2011, 27:99-107. 10.5625/lar.2011.27.2.99, 3145995, 21826169.
31. Bao X, Faris AE, Jang EK, Haslam RJ. Molecular cloning, bacterial expression and properties of Rab31 and Rab32. Eur J Biochem 2002, 269:259-271. 10.1046/j.0014-2956.2001.02645.x, 11784320.
32. Gao CF, Xie Q, Su YL, Koeman J, Khoo SK, Gustafson M, Knudsen BS, Hay R, Shinomiya N, Vande Woude GF. Proliferation and invasion: plasticity in tumor cells. Proc Natl Acad Sci U S A 2005, 102:10528-10533. 10.1073/pnas.0504367102, 1180792, 16024725.
33. Kauppi M, Simonsen A, Bremnes B, Vieira A, Callaghan J, Stenmark H, Olkkonen VM. The small GTPase Rab22 interacts with EEA1 and controls endosomal membrane trafficking. J Cell Sci 2002, 115:899-911.
34. Heinonen M, Fagerholm R, Aaltonen K, Kilpivaara O, Aittomaki K, Blomqvist C, Heikkila P, Haglund C, Nevanlinna H, Ristimaki A. Prognostic role of HuR in hereditary breast cancer. Clin Cancer Res 2007, 13:6959-6963. 10.1158/1078-0432.CCR-07-1432, 18056170.
35. Heinonen M, Bono P, Narko K, Chang SH, Lundin J, Joensuu H, Furneaux H, Hla T, Haglund C, Ristimaki A. Cytoplasmic HuR expression is a prognostic factor in invasive ductal breast carcinoma. Cancer Res 2005, 65:2157-2161. 10.1158/0008-5472.CAN-04-3765, 15781626.
36. Srikantan S, Gorospe M. HuR function in disease. Front Biosci 2012, 17:189-205. 10.2741/3921, 22201738.
37. Gubin MM, Calaluce R, Davis JW, Magee JD, Strouse CS, Shaw DP, Ma L, Brown A, Hoffman T, Rold TL, Atasoy U. Overexpression of the RNA binding protein HuR impairs tumor growth in triple negative breast cancer associated with deficient angiogenesis. Cell Cycle 2010, 9:3337-3346. 10.4161/cc.9.16.12711, 3041167, 20724828.
38. Chen CZ, Collins RN. Insights into biological functions across species: examining the role of Rab proteins in YIP1 family function. Biochem Soc Trans 2005, 33:614-618. 10.1042/BST0330614, 16042556.
39. Chavez CA, Bohnsack RN, Kudo M, Gotschall RR, Canfield WM, Dahms NM. Domain 5 of the cation-independent mannose 6-phosphate receptor preferentially binds phosphodiesters (mannose 6-phosphate N-acetylglucosamine ester). Biochemistry 2007, 46:12604-12617. 10.1021/bi7011806, 17927214.
40. Bohnsack RN, Song X, Olson LJ, Kudo M, Gotschall RR, Canfield WM, Cummings RD, Smith DF, Dahms NM. Cation-independent mannose 6-phosphate receptor: a composite of distinct phosphomannosyl binding sites. J Biol Chem 2009, 284:35215-35226. 10.1074/jbc.M109.056184, 2787381, 19840944.
41. Kim JJ, Olson LJ, Dahms NM. Carbohydrate recognition by the mannose-6-phosphate receptors. Curr Opin Struct Biol 2009, 19:534-542. 10.1016/j.sbi.2009.09.002, 2771201, 19801188.
42. Sleat DE, Lobel P. Ligand binding specificities of the two mannose 6-phosphate receptors. J Biol Chem 1997, 272:731-738. 10.1074/jbc.272.2.731, 8995357.
43. Dahms NM, Wick DA, Brzycki-Wessell MA. The bovine mannose 6-phosphate/insulin-like growth factor II receptor. Localization of the insulin-like growth factor II binding site to domains 5-11. J Biol Chem 1994, 269:3802-3809.
44. Dahms NM, Hancock MK. P-type lectins. Biochim Biophys Acta 2002, 1572:317-340. 10.1016/S0304-4165(02)00317-3, 12223278.
45. Nykjaer A, Christensen EI, Vorum H, Hager H, Petersen CM, Roigaard H, Min HY, Vilhardt F, Moller LB, Kornfeld S, Gliemann J. Mannose 6-phosphate/insulin-like growth factor-II receptor targets the urokinase receptor to lysosomes via a novel binding interaction. J Cell Biol 1998, 141:815-828. 10.1083/jcb.141.3.815, 2132758, 9566979.
46. Kreiling JL, Byrd JC, Deisz RJ, Mizukami IF, Todd RF, MacDonald RG. Binding of urokinase-type plasminogen activator receptor (uPAR) to the mannose 6-phosphate/insulin-like growth factor II receptor: contrasting interactions of full-length and soluble forms of uPAR. J Biol Chem 2003, 278:20628-20637. 10.1074/jbc.M302249200, 12665524.
47. Olson LJ, Yammani RD, Dahms NM, Kim JJ. Structure of uPAR, plasminogen, and sugar-binding sites of the 300 kDa mannose 6-phosphate receptor. Embo J 2004, 23:2019-2028. 10.1038/sj.emboj.7600215, 424385, 15085180.
48. Schiller HB, Szekeres A, Binder BR, Stockinger H, Leksa V. Mannose 6-phosphate/insulin-like growth factor 2 receptor limits cell invasion by controlling alphaVbeta3 integrin expression and proteolytic processing of urokinase-type plasminogen activator receptor. Mol Biol Cell 2009, 20:745-756. 2633380, 19037107.
49. Kotzsch M, Farthmann J, Meye A, Fuessel S, Baretton G, Tjan-Heijnen VC, Schmitt M, Luther T, Sweep FC, Magdolen V, Span PN. Prognostic relevance of uPAR-del4/5 and TIMP-3 mRNA expression levels in breast cancer. Eur J Cancer 2005, 41:2760-2768. 10.1016/j.ejca.2005.09.002, 16256342.
50. Tran H, Maurer F, Nagamine Y. Stabilization of urokinase and urokinase receptor mRNAs by HuR is linked to its cytoplasmic accumulation induced by activated mitogen-activated protein kinase-activated protein kinase 2. Mol Cell Biol 2003, 23:7177-7188. 10.1128/MCB.23.20.7177-7188.2003, 230330, 14517288.
51. Debela M, Magdolen V, Schechter N, Valachova M, Lottspeich F, Craik CS, Choe Y, Bode W, Goettig P. Specificity profiling of seven human tissue kallikreins reveals individual subsite preferences. J Biol Chem 2006, 281:25678-25688. 10.1074/jbc.M602372200, 16740631.
52. Rettenberger P, Wilhelm O, Oi H, Weidle UH, Goretzki L, Koppitz M, Lottspeich F, Konig B, Pessara U, Kramer MD, Schmitt M, Magdolen V. A competitive chromogenic assay to study the functional interaction of urokinase-type plasminogen activator with its receptor. Biol Chem Hoppe Seyler 1995, 376:587-594. 10.1515/bchm3.1995.376.10.587, 8590627.
53. Luther T, Magdolen V, Albrecht S, Kasper M, Riemer C, Kessler H, Graeff H, Muller M, Schmitt M. Epitope-mapped monoclonal antibodies as tools for functional and morphological analyses of the human urokinase receptor in tumor tissue. Am J Pathol 1997, 150:1231-1244. 1858180, 9094980.
54. Krüger A, Soeltl R, Sopov I, Kopitz C, Arlt M, Magdolen V, Harbeck N, Gänsbacher B, Schmitt M. Hydroxamate-type matrix metalloproteinase inhibitor batimastat promotes liver metastasis. Cancer Res 2001, 61:1272-1275.
55. Kopitz C, Anton M, Gänsbacher B, Krüger A. Reduction of experimental human fibrosarcoma lung metastasis in mice by adenovirus-mediated cystatin C overexpression in the host. Cancer Res 2005, 65:8608-8612. 10.1158/0008-5472.CAN-05-1572, 16204025.
56. Krüger A, Schirrmacher V, Khokha R. The bacterial lacZ gene: an important tool for metastasis research and evaluation of new cancer therapies. Cancer Metastasis Rev 1998, 17:285-294. 10.1023/A:1006066706040, 10352882.