Behind the scenes: Endo/exocytosis in the acquisition of metastatic traits

Cancer Research

Volumn 77, Issue 8, 2017, Pages 1813-1817

  Lanzetti, Letizia ^a,b   Di Fiore, Pier Paolo ^c,d,e  

^a CANDIOLO CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

^e EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CBL PROTEIN; CLATHRIN; DYNAMIN II; ENDOPHILIN; INTEGRIN; METALLOPROTEINASE; NOTCH RECEPTOR; PROTEIN CDC42; PROTEIN P53; RAB PROTEIN; SYNAPTOJANIN; TENSIN; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN; WNT PROTEIN;

ANOIKIS; BREAST CANCER; CARCINOGENESIS; CELL MIGRATION; CELL MOTILITY; COLORECTAL CANCER; CYTOSKELETON; ENDOCYTOSIS; ENVIRONMENTAL STRESS; EPITHELIAL MESENCHYMAL TRANSITION; EXOCYTOSIS; GENE OVEREXPRESSION; HUMAN; METASTASIS; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; REVIEW; SURVIVAL; TUMOR GROWTH; TUMOR INVASION; ANIMAL; CELL MEMBRANE; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CARCINOGENESIS; CELL MEMBRANE; ENDOCYTOSIS; EXOCYTOSIS; HUMANS; NEOPLASM METASTASIS; NEOPLASMS; RAB GTP-BINDING PROTEINS;

EID: 85018828629     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-3403     Document Type: Review

References (48)

1. Sigismund S, Confalonieri S, Ciliberto A, Polo S, Scita G, Di Fiore PP. Endocytosis and signaling: cell logistics shape the eukaryotic cell plan. Physiol Rev 2012;92:273-366.
2. Mellman I, Yarden Y. Endocytosis and cancer. Cold Spring Harb Perspect Biol 2013;5:a016949.
3. Venet D, Dumont JE, Detours V. Most random gene expression signatures are significantly associated with breast cancer outcome. PLoS Comput Biol 2011;7:e1002240.
4. Paul CD, Mistriotis P, Konstantopoulos K. Cancer cell motility: lessons from migration in confined spaces. Nat Rev Cancer 2017;17:131-40.
5. Palamidessi A, Frittoli E, Garre M, Faretta M, Mione M, Testa I, et al. Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 2008;134:135-47.
6. Wandinger-Ness A, Zerial M. Rab proteins and the compartmentalization of the endosomal system. Cold SpringHarb Perspect Biol 2014;6:a022616.
7. Frittoli E, Palamidessi A, Marighetti P, Confalonieri S, Bianchi F, Malinverno C, et al. A RAB5/RAB4 recycling circuitry induces a proteolytic invasive program and promotes tumor dissemination. J Cell Biol 2014;206:307-28.
8. Ferguson SM, De Camilli P. Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol 2012;13:75-88.
9. Eppinga RD, Krueger EW, Weller SG, Zhang L, Cao H, McNiven MA. Increased expression of the large GTPase dynamin 2 potentiates metastatic migration and invasion of pancreatic ductal carcinoma. Oncogene 2012;31:1228-41.
10. Razidlo GL, Wang Y, Chen J, Krueger EW, Billadeau DD, McNiven MA. Dynamin 2 potentiates invasive migration of pancreatic tumor cells through stabilization of the Rac1 GEF Vav1. Dev Cell 2013;24:573-85.
11. Fernandez-Zapico ME, Gonzalez-Paz NC, Weiss E, Savoy DN, Molina JR, Fonseca R, et al. Ectopic expression of VAV1 reveals an unexpected role in pancreatic cancer tumorigenesis. Cancer Cell 2005;7:39-49.
12. Chuang YY, Tran NL, Rusk N, Nakada M, Berens ME, Symons M. Role of synaptojanin 2 in glioma cell migration and invasion. Cancer Res 2004; 64:8271-5.
13. Ben-Chetrit N, Chetrit D, Russell R, Körner C, Mancini M, Abdul-Hai A, et al. Synaptojanin 2 is a druggable mediator of metastasis and the gene is overexpressed and amplified in breast cancer. Sci Signal 2015;8:ra7.
14. Frost A, Unger VM, De Camilli P. The BAR domain superfamily: membrane-molding macromolecules. Cell 2009;137:191-6.
15. Chander H, Truesdell P, Meens J, Craig AW. Transducer of Cdc42-dependent actin assembly promotes breast cancer invasion and metastasis. Oncogene 2013;32:3080-90.
16. Rolland Y, Marighetti P, Malinverno C, Confalonieri S, Luise C, Ducano N, et al. The CDC42-interacting protein 4 controls epithelial cell cohesion and tumor dissemination. Dev Cell 2014;30:553-68.
17. Cheng KW, Lahad JP, Kuo WL, Lapuk A, Yamada K, Auersperg N, et al. The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers. Nat Med 2004;10:1251-6.
18. Caswell PT, Spence HJ, Parsons M, White DP, Clark K, Cheng KW, et al. Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments. Dev Cell 2007;13:496-510.
19. Mitra S, Cheng KW, Mills GB. Rab25 in cancer: A brief update. Biochem Soc Trans 2012;40:1404-8.
20. Cheng KW, Agarwal R, Mitra S, Lee JS, Carey M, Gray JW, et al. Rab25 increases cellular ATP and glycogen stores protecting cancer cells from bioenergetic stress. EMBO Mol Med 2012;4:125-41.
21. Rainero E, Howe JD, Caswell PT, Jamieson NB, Anderson K, Critchley DR, et al. Ligand-occupied integrin internalization links nutrient signaling to invasive migration. Cell Rep 2015;10:398-413.
22. Nam KT, Lee HJ, Smith JJ, Lapierre LA, Kamath VP, Chen X, et al. Loss of Rab25 promotes the development of intestinal neoplasia in mice and is associated with human colorectal adenocarcinomas. J Clin Invest 2010;120:840-9.
23. Jones RG, Li X, Gray PD, Kuang J, Clayton F, Samowitz WS, et al. Conditional deletion of beta1 integrins in the intestinal epithelium causes a loss of Hedgehog expression, intestinal hyperplasia, and early postnatal lethality. J Cell Biol 2006;175:505-14.
24. Dozynkiewicz MA, Jamieson NB, Macpherson I, Grindlay J, van den Berghe PV, von Thun A, et al. Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression. Dev Cell 2012;22:131-45.
25. Caswell PT, Chan M, Lindsay AJ, McCaffrey MW, Boettiger D, Norman JC. Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J Cell Biol 2008;183:143-55.
26. Zhang J, Liu X, Datta A, Govindarajan K, Tam WL, Han J, et al. RCP is a human breast cancer-promoting gene with Ras-activating function. J Clin Invest 2009;119:2171-83.
27. Muller PA, Caswell PT, Doyle B, Iwanicki MP, Tan EH, Karim S, et al. Mutant p53 drives invasion by promoting integrin recycling. Cell 2009;139:1327-41.
28. Thomas JD, Zhang YJ, Wei YH, Cho JH, Morris LE, Wang HY, et al. Rab1A is an mTORC1 activator and a colorectal oncogene. Cancer Cell 2014;26: 754-69.
29. Nieto MA, Huang RY, Jackson RA, Thiery JP. EMT: 2016. Cell 2016;166: 21-45.
30. Chaffer CL, San Juan BP, Lim E, Weinberg RA. EMT, cell plasticity and metastasis. Cancer Metastasis Rev 2016;35:645-54.
31. Corallino S, Malabarba MG, Zobel M, Di Fiore PP, Scita G. Epithelial-tomesenchymal plasticity harnesses endocytic circuitries. Front Oncol 2015;5:45.
32. Pece S, Confalonieri S, R Romano P, Di Fiore PP. NUMB-ing down cancer by more than just a NOTCH. Biochim Biophys Acta 2011;1815:26-43.
33. Colaluca IN, Tosoni D, Nuciforo P, Senic-Matuglia F, Galimberti V, VialeG, et al. NUMB controls p53 tumour suppressor activity. Nature 2008; 451:76-80.
34. Tosoni D, Zecchini S, Coazzoli M, Colaluca I, Mazzarol G, Rubio A, et al. The Numb/p53 circuitry couples replicative self-renewal and tumor suppression in mammary epithelial cells. J Cell Biol 2015;211:845-62.
35. Wang Z, Sandiford S, Wu C, Li SS. Numb regulates cell-cell adhesion and polarity in response to tyrosine kinase signalling. EMBO J 2009;28: 2360-73.
36. Kandachar V, Roegiers F. Endocytosis and control of Notch signaling. Curr Opin Cell Biol 2012;24:534-40.
37. Kotiyal S, Bhattacharya S. Breast cancer stem cells, EMT and therapeutic targets. Biochem Biophys Res Commun 2014;453:112-6.
38. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009;138:1083-95.
39. Luo ML, Gong C, Chen CH, Hu H, Huang P, Zheng M, et al. The Rab2A GTPase promotes breast cancer stem cells and tumorigenesis via Erk signaling activation. Cell Rep 2015;11:111-24.
40. Kajiho H, Kajiho Y, Frittoli E, Confalonieri S, Bertalot G, Viale G, et al. RAB2A controls MT1-MMP endocytic and E-cadherin polarized Golgi trafficking to promote invasive breast cancer programs. EMBO Rep 2016;17:1061-80.
41. Tisdale EJ, Bourne JR, Khosravi-Far R, Der CJ, Balch WE. GTP-binding mutants of rab1 and rab2 are potent inhibitors of vesicular transport from the endoplasmic reticulum to the Golgi complex. J Cell Biol 1992; 119:749-61.
42. Gillingham AK, Sinka R, Torres IL, Lilley KS, Munro S. Toward a comprehensive map of the effectors of rab GTPases. Dev Cell 2014;31:358-73.
43. Spang A. Membrane tethering complexes in the endosomal system. Front Cell Dev Biol 2016;4:35.
44. Luo ML, Gong C, Chen CH, Lee DY, Hu H, Huang P, et al. Prolyl isomerase Pin1 acts downstream of miR200c to promote cancer stem-like cell traits in breast cancer. Cancer Res 2014;74:3603-16.
45. Rustighi A, Zannini A, Tiberi L, Sommaggio R, Piazza S, Sorrentino G, et al. Prolyl-isomerase Pin1 controls normal and cancer stem cells of the breast. EMBO Mol Med 2014;6:99-119.
46. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, MaoM, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002;415:530-6.
47. Waclaw B, Bozic I, Pittman ME, Hruban RH, Vogelstein B, Nowak MA. A spatial model predicts that dispersal and cell turnover limit intratumour heterogeneity. Nature 2015;525:261-4.
48. Mills GB, Jurisica I, Yarden Y, Norman JC. Genomic amplicons target vesicle recycling in breast cancer. J Clin Invest 2009;119:2123-7.