Control of MT1-MMP transport by atypical PKC during breast-cancer progression

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 18, 2014, Pages

  Rossé, Carine ^a,b   Lodillinsky, Catalina ^a,b   Fuhrmann, Laetitia ^a   Nourieh, Maya ^a   Monteiro, Pedro ^a,b,c   Irondelle, Marie ^a,b   Lagoutte, Emilie ^a,b   Vacher, Sophie ^a   Waharte, François ^a,b   Paul Gilloteaux, Perrine ^a,b   Romao, Maryse ^a,b   Sengmanivong, Lucie ^a,b   Linch, Mark ^d   Van Lint, Johan ^e   Raposo, Graça ^a,b   Vincent Salomon, Anne ^a,f   Bièche, Ivan ^a   Parker, Peter J ^d,g   Chavrier, Philippe ^a,b  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^e UNIVERSITY OF LEUVEN   (Belgium)

^f INSERM   (France)

^g KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Actin cytoskeleton; Membrane traffic; MMP14; Multi vesicular body

Indexed keywords

CORTACTIN; DYNAMIN II; MATRIX METALLOPROTEINASE 14; PROTEIN KINASE C IOTA;

ARTICLE; BREAST CANCER; CANCER GROWTH; CARCINOMA CELL; CELL MEMBRANE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOSOME; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; TRIPLE NEGATIVE BREAST CANCER; UPREGULATION;

ACTIN CYTOSKELETON; MEMBRANE TRAFFIC; MMP14; MULTI-VESICULAR BODY;

ADENOCARCINOMA; ADULT; AGED; BIOLOGICAL TRANSPORT, ACTIVE; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; CORTACTIN; CYTOPLASMIC GRANULES; DISEASE PROGRESSION; DYNAMIN II; ENDOSOMES; EXTRACELLULAR MATRIX; FEMALE; HUMANS; ISOENZYMES; MATRIX METALLOPROTEINASE 14; MIDDLE AGED; NEOPLASM INVASIVENESS; PHOSPHORYLATION; PROTEIN KINASE C; RNA INTERFERENCE; RNA, MESSENGER; RNA, NEOPLASM; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 84899800579     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400749111     Document Type: Article

References (54)

1. Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2(3):161-174.
2. Kessenbrock K, Plaks V, Werb Z (2010) Matrix metalloproteinases: Regulators of the tumor microenvironment. Cell 141(1):52-67.
3. Sato H, et al. (1994) A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370(6484):61-65.
4. Strongin AY, et al. (1995) Mechanism of cell surface activation of 72-kDa type IV collagenase: Isolation of the activated form of the membrane metalloprotease. J Biol Chem 270(10):5331-5338.
5. Hotary KB, et al. (2003) Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114(1): 33-45.
6. Hotary K, Li XY, Allen E, Stevens SL, Weiss SJ (2006) A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev 20(19): 2673-2686.
7. Wolf K, et al. (2007) Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 9(8):893-904.
8. Jiang WG, et al. (2006) Expression of membrane type-1 matrix metalloproteinase, MT1-MMP in human breast cancer and its impact on invasiveness of breast cancer cells. Int J Mol Med 17(4):583-590.
9. Perentes JY, et al. (2011) Cancer cell-associated MT1-MMP promotes blood vessel invasion and distant metastasis in triple-negative mammary tumors. Cancer Res 71(13):4527-4538.
10. Art ym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC (2006) Dynamic interactions of cortactin and membrane type matrix metalloproteinase at invadopodia: Defining the stages of invadopodia formation and function. Cancer Res 66(6):3034-3043.
11. Murphy DA, Courtneidge SA (2011) The ?ins? and ?outs? of podosomes and invadopodia: Characteristics, formation and function. Nat Rev Mol Cell Biol 12(7): 413-426.
12. Poincloux R,Lizárraga F,Chavrier P(2009) Matrix invasion by tumour cells: A focus on MT1-MMP trafficking to invadopodia. J Cell Sci, 122(Pt 17) 3015-3024.
13. Steffen A, et al. (2008) MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7. Curr Biol 18(12):926-931.
14. Clark ES, Whigham AS, Yarbrough WG, Weaver AM (2007) Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res 67(9):4227-4235.
15. Sakurai-Yageta M, et al. (2008) Th e interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J Cell Biol 181(6): 985-998.
16. Williams KC, Coppolino MG (2011) Phosphorylation of me mbrane type 1-matrix metalloproteinase (MT1-MMP) and its vesicle-associated membrane protein 7 (VAMP7)-dependent trafficking facilitate cell invasion and migration. J Biol Chem 286(50):43405-43416.
17. Mellor H, Parker PJ (1998) The extended protein kinase C superfamily. Biochem J 332(Pt 2):281-292.
18. McCaffrey LM, Macara IG (2011) Epithelial organization, cell polarity and tumorigenesis. Trends Cell Biol 21(12):727-735.
19. Rosse C, et al. (2009) An aPKC-exocyst complex controls paxillin phosphorylation and migration through localised JNK1 activation. PLoS Biol 7(11):e1000235.
20. Sun R, et al. (2005) Protein kinase C zeta is required for epidermal growth factorinduced chemotaxis of human breast cancer cells. Cancer Res 65(4):1433-1441.
21. Rodriguez EM, Dunham EE, Martin GS (2009) Atypical protein kinase C activity is required for extracellular matrix degradation and invasion by Src-transformed cells. J Cell Physiol 221(1):171-182.
22. Kojima Y, et al. (2008) The overex pression and altered localization of the atypical protein kinase C lambda/iota in breast cancer correlates with the pathologic type of these tumors. Hum Pathol 39(6):824-831.
23. Awadelkarim KD, et al. (2012 ) Quantification of PKC family genes in sporadic breast cancer by qRT-PCR: Evidence that PKC/ overexpression is an independent prognostic factor. Int J Cancer 131(12):2852-2862.
24. Regala RP, et al. (2005) Atypical protein kinase C iota is an oncogene in human nonsmall cell lung cancer. Cancer Res 65(19):8905-8911.
25. Sø rlie T, et al. (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 98(19):10869-10874.
26. Neve RM, et al. (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10(6):515-527.
27. Sabeh F, Shimizu-Hirota R, Weiss SJ (2009) Protease-dependent versus -independent cancer cell invasion programs: Three-dimensional amo eboid movement revisited. J Cell Biol 185(1):11-19.
28. Lizá rraga F, et al. (2009) Diaphanous-related formins are required for invadopodia formation and invasion of breast tumor cells. Cancer Res 69(7):2792-2800.
29. Miesenbock G (2012) Synapto-pHluorins: Genetically encoded reporters of synaptic transmission. Cold Spring Harb Protoc 2012(2):213-217.
30. De rivery E, et al. (2009) The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev Cell 17(5):712-723.
31. Puthenveedu MA, et al. (2010) Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143(5):761-773.
32. Sung BH, Zhu X, Kaverina I, Weaver AM (2011) Cortactin controls cell motility and lamellipodial dynamics by regulating ECM secretion. Curr Biol 21(17):1460-1469.
33. McNiven MA, et al. (2000) Regulated interactions between dynamin and the actinbinding protein cortactin modulate cell shape. J Cell Biol 151(1):187-198.
34. Baldassarre M, et al. (2003) Dynamin participates in focal extracellular matrix degradation by invasive cells. Mol Biol Cell 14(3):1074-1084.
35. Eiseler T, Hausser A, De Kimpe L, Van Lint J, Pfizenmaier K (2010) Protein kinase D controls actin polymerization and cell motility through phosphorylation of cortactin. J Biol Chem 285(24):18672-18683.
36. Rozengurt E (2011) Protein kinase D signaling: Multiple biological functions in health and disease. Physiology (Bethesda) 26(1):23-33.
37. van Rossum AG, Schuuring-Scholtes E, van Buuren-van Seggelen V, Kluin PM, Schuuring E (2005) Comparative gen ome analysis of cortactin and HS1: The significance of the F-actin binding repeat domain. BMC Genomics 6:15.
38. Dozynkiewicz MA, et al. (2012) Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression. Dev Cell 22(1): 131-145.
39. Schroeder B, Weller SG, Chen J, Billadeau D, McNiven MA (2010) A Dyn2-CIN85 complex mediates degradative t raffic of the EGFR by regulation of late endosomal budding. EMBO J 29(18):3039-3053.
40. Harrington AW, et al. (2011) Recruitment of actin modifiers to TrkA endosomes governs retrograde NGF signaling and survival. Cell 146(3):421-434.
41. Luo ML, et al. (2006) Amplification and overexpression of CTTN (EMS1) contribute to the metastasis of esophageal squamous cell carcinoma by promoting cell migrat ion and anoikis resistance. Cancer Res 66(24):11690-11699.
42. Clark ES, et al. (2009) Aggressiveness of HNSCC tumors depends on expression levels of cortactin, a gene in the 11q13 amplicon. Oncogene 28(3):431-444.
43. Eppinga RD, et al. (2012) Increased expression of the large GTPase dynamin potentiates metastatic migration and invasion of pancreatic ductal carcinoma. Oncogene 31(10):1228-1241.
44. Huang L, Muthuswamy SK (2010) Polarity protein alterations in carcinoma: A focus on emerging roles for polarity regulators. Curr Opin Genet Dev 20(1):41-50.
45. Leibfried A, Fricke R, Morgan MJ, Bogdan S, Bellaiche Y (2008) Drosophila Cip4 and WASp define a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis. Curr Biol 18( 21):1639-1648.
46. Winter JF, et al. (2012) Caenorhabditis elegans screen reveals role of PAR-5 in RAB-11- recycling endosome positioning and apicobasal cell polarity. Nat Cell Biol 14(7): 666-676.
47. Nolan ME, et al. (2008) The polarity protein Par6 induces cell proliferation and is overexpressed in breast cancer. Cancer Res 68(20):8201-8209.
48. McCaffrey LM, Montalbano J, Mihai C, Macara IG (2012) Loss of the Par3 polarity protein promotes breast tumorigenesis and metastasis. Cancer Cell 22(5):601-614.
49. Xue B, Krishnamurthy K, Allred DC, Muthuswamy SK (2013) Loss of Par3 promotes breast cancer metastasis by compromising cell-cell cohesion. Nat Cell Biol 15(2): 189-200.
50. Rey M, Irondelle M, Waharte F, Lizarraga F, Chavrier P (2011) HDAC6 is required for invadopodia activity and invasion by breast tumor cells. Eur J Cell Biol 90(2 -3): 128-135.
51. Montagnac G, et al. (2011) Decoupling of activation and effector binding underlies ARF6 priming of fast endocytic recycling. Curr Biol 21(7):574-579.
52. Prat A, et al. (2013) Prognostic significance of progesterone receptor-positive tumor cells within immunohistochemically defined luminal A breast cancer. J Clin Oncol 31(2):203-209.
53. Wolff AC, et al. (2007) American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor testing in breast cancer. J Clin Oncol, 25(1): 118-145.
54. Vincent-Salomon A, et al. (2007) HER2 status of bone marrow micrometastasis and their corresponding primary tumours in a pilot study of cases: A possible tool for anti-HER2 ther apy management Br J Cancer 96(4):654-659.