The mannose 6-phosphate/insulin-like growth factor II receptor restricts the tumourigenicity and invasiveness of squamous cell carcinoma cells

International Journal of Cancer

Volumn 124, Issue 11, 2009, Pages 2559-2567

  Probst, Olivia C ^a   Puxbaum, Verena ^a   Svoboda, Barbara ^a   Leksa, Vladimir ^b,c   Stockinger, Hannes ^b   Mikula, Mario ^d,e   Mikulits, Wolfgang ^d   Mach, Lukas ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c INSTITUTE OF CHEMISTRY   (Slovakia)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e Universitatsklinik fur Dermatologie   (Austria)

Author keywords

Cathepsin; Lysosome; Proteolysis; Squamous cell carcinoma; Tumour invasion

Indexed keywords

CHEMOATTRACTANT; COMPLEMENTARY DNA; MANNOSE 6 PHOSPHATE; SOMATOMEDIN B RECEPTOR; BETA N ACETYLHEXOSAMINIDASE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER INVASION; CARCINOGENICITY; CARCINOMA CELL; CONTROLLED STUDY; GENETIC TRANSFECTION; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SQUAMOUS CELL CARCINOMA; ANIMAL; CELL PROLIFERATION; ENZYMOLOGY; EXTRACELLULAR MATRIX; FEMALE; HUMAN; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BETA-N-ACETYLHEXOSAMINIDASES; CARCINOMA, SQUAMOUS CELL; CELL PROLIFERATION; EXTRACELLULAR MATRIX; FEMALE; HUMANS; LYSOSOMES; MICE; MICE, SCID; NEOPLASM INVASIVENESS; RECEPTOR, IGF TYPE 2; TUMOR SUPPRESSOR PROTEINS;

EID: 64249094725     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24236     Document Type: Article

References (49)

1. Stetler-Stevenson WG, Aznavoorian S, Liotta LA. Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu Rev Cell Biol 1993;9:541-573
2. Liotta LA, Kohn EC. The microenvironment of the tumour-host interface. Nature 2001;411:375-379
3. Sidenius N, Blasi F. The urokinase plasminogen activator system in cancer: recent advances and implication for prognosis and therapy. Cancer Metastasis Rev 2003;22:205-222 (Pubitemid 36561058)
4. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 2006;25:9-34. (Pubitemid 43723979)
5. Mohamed MM, Sloane BF. Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer 2006;6:764-775 (Pubitemid 44450465)
6. Poole AR, Tiltman KJ, Recklies AD, Stoker TA. Differences in secretion of the proteinase cathepsin B at the edges of human breast carcinomas and fibroadenomas. Nature 1978;273:545-547 (Pubitemid 8346587)
7. Ghosh P, Dahms NM, Kornfeld S. Mannose 6-phosphate receptors: new twists in the tale. Nat Rev Mol Cell Biol 2003;4:202-212 (Pubitemid 36288042)
8. Achkar C, Gong QM, Frankfater A, Bajkowski AS. Differences in targeting and secretion of cathepsins B and L by BALB/3T3 fibroblasts and Moloney murine sarcoma virus-transformed BALB/3T3 fibroblasts. J Biol Chem 1990;265:13650-13654 (Pubitemid 20252219)
9. Capony F, Braulke T, Rougeot C, Roux S, Montcourrier P, Rochefort H. Specific mannose-6-phosphate receptor-independent sorting of pro-cathepsin D in breast cancer cells. Exp Cell Res 1994;215:154-163 (Pubitemid 24339186)
10. Lorenzo K, Ton P, Clark JL, Coulibaly S, Mach L. Invasive properties of murine squamous carcinoma cells: secretion of matrix-degrading cathepsins is attributable to a deficiency in the mannose 6-phosphate/ insulin-like growth factor II receptor. Cancer Res 2000;60:4070-4076 (Pubitemid 30636587)
11. Ludwig T, Munier-Lehmann H, Bauer U, Hollinshead M, Ovitt C, Lobel P, Hoflack B. Differential sorting of lysosomal enzymes in mannose 6-phosphate receptor-deficient fibroblasts. EMBO J 1994;13:3430-3437 (Pubitemid 24246178)
12. Pohlmann R, Wendland M, Boeker C, von Figura K. The two mannose 6-phosphate receptors transport distinct complements of lysosomal proteins. J Biol Chem 1995;270:27311-27318
13. Kiess W, Blickenstaff GD, Sklar MM, Thomas CL, Nissley SP, Sahagian GG. Biochemical evidence that the type II insulin-like growth factor receptor is identical to the cation-independent mannose 6-phosphate receptor. J Biol Chem 1988;263:9339-9344 (Pubitemid 18160210)
14. Kovacina KS, Steele-Perkins G, Purchio AF, Lioubin M, Miyazono K, Heldin CH, Roth RA. Interactions of recombinant and platelet transforming growth factor-b1 precursor with the insulin-like growth factor II/mannose 6-phosphate receptor. Biochem Biophys Res Commun 1989;160:393-403. (Pubitemid 19116510)
15. 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 (Pubitemid 28217924)
16. Godar S, Horejsi V, Weidle UH, Binder BR, Hansmann C, Stockinger H. M6P/IGFII-receptor complexes urokinase receptor and plasminogen for activation of transforming growth factor-β1. Eur J Immunol 1999;29:1004-1013 (Pubitemid 29119081)
17. Jirtle RL. Genomic imprinting and cancer. Exp Cell Res 1999;248:18-24. (Pubitemid 29393925)
18. Kong FM, Anscher MS, Washington MK, Killian JK, Jirtle RL. M6P/ IGF2R is mutated in squamous cell carcinoma of the lung. Oncogene 2000;19:1572-1578 (Pubitemid 30175679)
19. Jamieson TA, Brizel DM, Killian JK, Oka Y, Jang H-S, Fu X, Clough RW, Vollmer RT, Anscher MS, Jirtle RL. M6P/IGF2R loss of heterozygosity in head and neck cancer associated with poor patient prognosis. BMC Cancer 2003;3:4. (Pubitemid 38851345)
20. Byrd JC, Devi GR, de Souza AT, Jirtle RL, MacDonald RG. Disruption of ligand binding to the insulin-like growth factor II/mannose-6- phosphate receptor by cancer-associated missense mutations. J Biol Chem 1999;274:24408-24416 (Pubitemid 129528494)
21. Devi GR, De Souza AT, Byrd JC, Jirtle RL, MacDonald RG. Altered ligand binding by insulin-like growth factor II/mannose-6-phosphate receptors bearing missense mutations in human cancer. Cancer Res 1999;59:4314-4319 (Pubitemid 29418749)
22. Wise TL, Pravtcheva DD. Delayed onset of Igf2-induced mammary tumors in Igf2r transgenic mice. Cancer Res 2006;66:1327-1336 (Pubitemid 43259911)
23. O'Gorman DB, Weiss J, Hettiaratchi A, Firth SM, Scott CD. Insulin-like growth factor-II/mannose 6-phosphate receptor overexpression reduces growth of choriocarcinoma cells in vitro and in vivo. Endocrinology 2002;143:4287-4294 (Pubitemid 35239560)
24. Lee JS, Weiss J, Martin JL, Scott CD. Increased expression of the mannose-6-phosphate/insulin-like growth factor-II receptor in breast cancer cells alters tumorigenic properties in vitro and in vivo. Int J Cancer 2003;107:564-570 (Pubitemid 37296116)
25. Li J, Sahagian GG. Demonstration of tumor suppression by mannose 6-phosphate/insulin-like growth factor 2 receptor. Oncogene 2004;23:9359-9368 (Pubitemid 40069668)
26. Souza RF, Wang S, Thakar M, Smolinski KN, Yin J, Zou TT, Kong D, Abraham JM, Toretsky JA, Meltzer SJ. Expression of the wild-type insulin- like growth factor II receptor gene suppresses growth and causes death in colorectal carcinoma cells. Oncogene 1999;18:4063-4068 (Pubitemid 29363913)
27. O'Gorman DB, Costello M, Weiss J, Firth SM, Scott CD. Decreased insulin-like growth factor-II/mannose 6-phosphate receptor expression enhances tumorigenicity in JEG-3 cells. Cancer Res 1999;59:5692-5694
28. Chen Z, Ge Y, Landman N, Kang JX. Decreased expression of the mannose 6-phosphate/insulin-like growth factor-II receptor promotes growth of human breast cancer cells. BMC Cancer 2002;2:18. (Pubitemid 38851303)
29. Coulibaly S, Schwihla H, Abrahamson M, Albini A, Cerni C, Clark JL, Ng KM, Katunuma N, Schlappack O, Glössl J, Mach L. Modulation of invasive properties of murine squamous carcinoma cells by heterologous expression of cathepsin B and cystatin C. Int J Cancer 1999;83:526-531 (Pubitemid 29489869)
30. Probst OC, Ton P, Svoboda B, Gannon A, Schuhmann W, Wieser J, Pohlmann R, Mach L. The 46-kDa mannose 6-phosphate receptor does not depend on endosomal acidification for delivery of hydrolases to lysosomes. J Cell Sci 2006;119:4935-4943 (Pubitemid 46017806)
31. Leksa V, Godar S, Cebecauer M, Hilgert I, Breuss J, Weidle UH, Horejsi V, Binder BR, Stockinger H. The N terminus of mannose 6-phosphate/ insulin-like growth factor 2 receptor in regulation of fibrinolysis and cell migration. J Biol Chem 2002;277:40575-40582 (Pubitemid 35215637)
32. Klumperman J, Hille A, Veenendaal T, Oorschot V, Stoorvogel W, von Figura K, Geuze HJ. Differences in the endosomal distributions of the two mannose 6-phosphate receptors. J Cell Biol 1993;121:997-1010. (Pubitemid 23154261)
33. Dennes A, Cromme C, Suresh K, Kumar NS, Eble JA, Hahnenkamp A, Pohlmann R. The novel Drosophila lysosomal enzyme receptor protein mediates lysosomal sorting in mammalian cells and binds mammalian and Drosophila GGA adaptors. J Biol Chem 2005;280:12849-12857 (Pubitemid 40491106)
34. Mach L, Stüwe K, Hagen A, Ballaun C, Glössl J. Proteolytic processing of cathepsin B. The role of the primary structure of the latent precursor and of the carbohydrate moiety for cell-type-specific molecular forms of the enzyme. Biochem J 1992;282:577-582
35. Schmid JA, Mach L, Paschke E, Glössl J. Accumulation of sialic acid in endocytic compartments interferes with the formation of mature lysosomes. J Biol Chem 1999;274:19063-19071
36. Albini A, Iwamoto Y, Kleinman HK, Martin GR, Aaronson SA, Kozlowski JM, McEwan RN. A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 1987;47:3239-3245 (Pubitemid 17082655)
37. Wenk J, Hille A, von Figura K. Quantitation of Mr 46,000 and Mr 300,000 mannose 6-phosphate receptors in human cells and tissues. Biochem Int 1991;23:723-732
38. 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 (Pubitemid 350060086)
39. Dong JM, Prence EM, Sahagian GG. Mechanism for selective secretion of a lysosomal protease by transformed mouse fibroblasts. J Biol Chem 1989;264:7377-7383 (Pubitemid 19119149)
40. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70. (Pubitemid 30046295)
41. De Souza AT, Hankins GR, Washington MK, Orton TC, Jirtle RL. M6P/IGF2R gene is mutated in human hepatocellular carcinomas with loss of heterozygosity. Nat Genet 1995;11:447-449
42. Yamada T, De Souza AT, Finkelstein S, Jirtle RL. Loss of the gene encoding mannose 6-phosphate/insulin-like growth factor receptor is an early event in liver carcinogenesis. Proc Natl Acad Sci USA 1997;94:10351-10355 (Pubitemid 27407045)
43. Hankins GR, De Souza AT, Bentley RC, Patel MR, Marks JR, Iglehart JD, Jirtle RL. M6P/IGF2 receptor: a candidate breast tumor suppressor gene. Oncogene 1996;12:2003-2009 (Pubitemid 26154672)
44. Schaffer BS, Lin MF, Byrd JC, Park JH, MacDonald RG. Opposing roles for the insulin-like growth factor (IGF)-II and mannose 6-phosphate (Man-6-P) binding activities of the IGF-II/Man-6-P receptor in the growth of prostate cancer cells. Endocrinology 2003;144:955-966 (Pubitemid 36262863)
45. Rosenthal EL, Johnson TM, Allen ED, Apel IJ, Punturieri A, Weiss SJ. Role of the plasminogen activator and matrix metalloproteinase systems in epidermal growth factor- and scatter factor-stimulated invasion of carcinoma cells. Cancer Res 1998;58:5221-5230 (Pubitemid 28521186)
46. Hotary K, Li XY, Allen E, Stevens SL, Weiss SJ. A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev 2006;20:2673-2686 (Pubitemid 44498378)
47. Joyce JA, Baruch A, Chehade K, Meyer-Morse N, Giraudo E, Tsai FY, Greenbaum DC, Hager JH, Bogyo M, Hanahan D. Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. Cancer Cell 2004;5:443-453 (Pubitemid 38610246)
48. Lakka SS, Gondi CS, Yanamandra N, Olivero WC, Dinh DH, Gujrati M, Rao JS. Inhibition of cathepsin B and MMP-9 gene expression in glioblastoma cell line via RNA interference reduces tumor cell invasion, tumor growth and angiogenesis. Oncogene 2004;23:4681-4689 (Pubitemid 38859457)
49. Gocheva V, Zeng W, Ke D, Klimstra D, Reinheckel T, Peters C, Hanahan D, Joyce JA. Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes Dev 2006;20:543-556 (Pubitemid 43345321)