Transgenic overexpression of the proprotein convertase furin enhances skin tumor growth

Neoplasia

Volumn 14, Issue 4, 2012, Pages 271-282

  Fu, Jian ^a   Bassi, Daniel E ^a   Zhang, Jirong ^a   Li, Tianyu ^a   Nicolas, Emmanuelle ^a   Klein Szanto, Andres J P ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FURIN; KI 67 ANTIGEN; PACE4 PROTEIN; PROPROTEIN CONVERTASE 2; PROPROTEIN CONVERTASE 5; PROPROTEIN CONVERTASE 7; SERINE PROTEINASE; SOMATOMEDIN C RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; EPIDERMIS; FEMALE; GENE EXPRESSION; GENOTYPE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN TUMOR; SQUAMOUS CELL CARCINOMA; TRANSGENIC MOUSE; TUMOR GROWTH; WESTERN BLOTTING;

EID: 84860621139     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.12166     Document Type: Article

References (51)

1. Seidah NG (2011). What lies ahead for the proprotein convertases? Ann N Y Acad Sci 1220, 149-161.
2. Seidah NG (2011). The proprotein convertases, 20 years later. Methods Mol Biol 768, 23-57.
3. Molloy SS, Anderson ED, Jean F, and Thomas G (1999). Bi-cycling the furin pathway: from TGN localization to pathogen activation and embryogenesis. Trends Cell Biol 9, 28-35.
4. Seidah NG, Benjannet S, Wickham L, Marcinkiewicz J, Jasmin SB, Stifani S, Basak A, Prat A, and Chretien M (2003). The secretory proprotein convertase neural apoptosis-regulated convertase 1 (NARC-1): liver regeneration and neuronal differentiation. Proc Natl Acad Sci USA 100, 928-933.
5. Seidah NG, Mowla SJ, Hamelin J, Mamarbachi AM, Benjannet S, Toure BB, Basak A, Munzer JS, Marcinkiewicz J, Zhong M, et al. (1999). Mammalian subtilisin/kexin isozyme SKI-1: a widely expressed proprotein convertase with a unique cleavage specificity and cellular localization. Proc Natl Acad Sci USA 96, 1321-1326.
6. Duguay SJ, Milewski WM, Young BD, Nakayama K, and Steiner DF (1997). Processing of wild-type and mutant proinsulin-like growth factor-IA by subtilisinrelated proprotein convertases. J Biol Chem 272, 6663-6670.
7. Lehmann M, Andre F, Bellan C, Remacle-Bonnet M, Garrouste F, Parat F, Lissitsky JC, Marvaldi J, and Pommier G (1998). Deficient processing and activity of type I insulin-like growth factor receptor in the furin-deficient LoVo-C5 cells. Endocrinology 139, 3763-3771.
8. Khatib AM, Siegfried G, Prat A, Luis J, Chretien M, Metrakos P, and Seidah NG (2001). Inhibition of proprotein convertases is associated with loss of growth and tumorigenicity of HT-29 human colon carcinoma cells: importance of insulin-like growth factor-1 (IGF-1) receptor processing in IGF-1-mediated functions. J Biol Chem 276, 30686-30693.
9. Stawowy P, Meyborg H, Stibenz D, Borges Pereira Stawowy N, Roser M, Thanabalasingam U, Veinot JP, Chretien M, Seidah NG, Fleck E, et al. (2005). Furin-like proprotein convertases are central regulators of the membrane type matrix metalloproteinase-pro-matrix metalloproteinase-2 proteolytic cascade in atherosclerosis. Circulation 111, 2820-2827.
10. Cao J, Rehemtulla A, Pavlaki M, Kozarekar P, and Chiarelli C (2005). Furin directly cleaves proMMP-2 in the trans-Golgi network resulting in a nonfunctioning proteinase. J Biol Chem 280, 10974-10980.
11. Wang P, Tortorella M, England K, Malfait AM, Thomas G, Arner EC, and Pei D (2004). Proprotein convertase furin interacts with and cleaves pro-ADAMTS4 (Aggrecanase-1) in the trans-Golgi network. J Biol Chem 279, 15434-15440.
12. Komiyama T, Coppola JM, Larsen MJ, Van Dort ME, Ross BD, Day R, Rehemtulla A, and Fuller RS (2009). Inhibition of furin/proprotein convertasecatalyzed surface and intracellular processing by small molecules. J Biol Chem 284, 15729-15738.
13. Yana I and Weiss SJ (2000). Regulation of membrane type-1 matrix metalloproteinase activation by proprotein convertases. Mol Biol Cell 11, 2387-2401.
14. 4 integrin by the proprotein convertases: histidine at position P6 regulates cleavage. Biochem J 373, 475-484.
15. V at specialized domains of renal cell plasma membrane. J Cell Sci 116, 1763-1773.
16. Smirnov SP, Mcdearmon EL, Li S, Ervasti JM, Tryggvason K, and Yurchenco PD (2002). Contributions of the LG modules and furin processing to laminin-2 functions. J Biol Chem 277, 18928-18937.
17. Lissitzky JC, Luis J, Munzer JS, Benjannet S, Parat F, Chretien M, Marvaldi J, and Seidah NG (2000). Endoproteolytic processing of integrin pro-α subunits involves the redundant function of furin and proprotein convertase (PC) 5A, but not paired basic amino acid converting enzyme (PACE) 4, PC5B or PC7. Biochem J 346(pt 1), 133-138.
18. Lehmann M, Rigot V, Seidah NG, Marvaldi J, and Lissitzky JC (1996). Lack of integrin α-chain endoproteolytic cleavage in furin-deficient human colon adenocarcinoma cells LoVo. Biochem J 317(pt 3), 803-809.
19. Khatib AM, Siegfried G, Chretien M, Metrakos P, and Seidah NG (2002). Proprotein convertases in tumor progression and malignancy: novel targets in cancer therapy. Am J Pathol 160, 1921-1935.
20. De Cicco RL, Bassi DE, Benavides F, Conti CJ, and Klein-Szanto AJ (2007). Inhibition of proprotein convertases: approaches to block squamous carcinoma development and progression. Mol Carcinog 46, 654-659.
21. Artenstein AW and Opal SM (2011). Proprotein convertases in health and disease. N Engl J Med 365, 2507-2518.
22. D'anjou F, Routhier S, Perreault JP, Latil A, Bonnel D, Fournier I, Salzet M, and Day R (2011). Molecular validation of PACE4 as a target in prostate cancer. Transl Oncol 4, 157-172.
23. Schalken JA, Roebroek AJ, Oomen PP, Wagenaar SS, Debruyne FM, Bloemers HP, and Van De Ven WJ (1987). fur gene expression as a discriminating marker for small cell and nonsmall cell lung carcinomas. J Clin Invest 80, 1545-1549.
24. Mbikay M, Sirois F, Yao J, Seidah NG, and Chretien M (1997). Comparative analysis of expression of the proprotein convertases furin, PACE4, PC1 and PC2 in human lung tumours. Br J Cancer 75, 1509-1514.
25. Bassi DE, Lopez De Cicco R, Mahloogi H, Zucker S, Thomas G, and Klein-Szanto AJ (2001). Furin inhibition results in absent or decreased invasiveness and tumorigenicity of human cancer cells. Proc Natl Acad Sci USA 98, 10326-10331.
26. Bassi DE, Mahloogi H, Al-Saleem L, Lopez De Cicco R, Ridge JA, and Klein-Szanto AJ (2001). Elevated furin expression in aggressive human head and neck tumors and tumor cell lines. Mol Carcinog 31, 224-232.
27. Bassi DE, Mahloogi H, Lopez De Cicco R, and Klein-Szanto A (2003). Increased furin activity enhances the malignant phenotype of human head and neck cancer cells. Am J Pathol 162, 439-447.
28. Lopez De Cicco R, Bassi DE, Zucker S, Seidah NG, and Klein-Szanto AJ (2005). Human carcinoma cell growth and invasiveness is impaired by the propeptide of the ubiquitous proprotein convertase furin. Cancer Res 65, 4162-4171.
29. Siegfried G, Khatib AM, Benjannet S, Chretien M, and Seidah NG (2003). The proteolytic processing of pro-platelet-derived growth factor-A at RRKR(86) by members of the proprotein convertase family is functionally correlated to plateletderived growth factor-A-induced functions and tumorigenicity. Cancer Res 63, 1458-1463.
30. Siegfried G, Basak A, Cromlish JA, Benjannet S, Marcinkiewicz J, Chretien M, Seidah NG, and Khatib AM (2003). The secretory proprotein convertases furin, PC5, and PC7 activate VEGF-C to induce tumorigenesis. J Clin Invest 111, 1723-1732.
31. Scamuffa N, Siegfried G, Bontemps Y, Ma L, Basak A, Cherel G, Calvo F, Seidah NG, and Khatib AM (2008). Selective inhibition of proprotein convertases represses the metastatic potential of human colorectal tumor cells. J Clin Invest 118, 352-363.
32. Lapierre M, Siegfried G, Scamuffa N, Bontemps Y, Calvo F, Seidah NG, and Khatib AM (2007). Opposing function of the proprotein convertases furin and PACE4 on breast cancer cells' malignant phenotypes: role of tissue inhibitors of metalloproteinase-1. Cancer Res 67, 9030-9034.
33. Basak A, Khatib AM, Mohottalage D, Basak S, Kolajova M, and Bag SS (2009). A novel enediynyl peptide inhibitor of furin that blocks processing of proPDGF-A, B and proVEGF-C. PLoS One 4, e7700.
34. Mercapide J, Lopez De Cicco R, Bassi DE, Castresana JS, Thomas G, and Klein-Szanto AJ (2002). Inhibition of furin-mediated processing results in suppression of astrocytoma cell growth and invasiveness. Clin Cancer Res 8, 1740-1746.
35. Bassi DE, Lopez De Cicco R, Cenna J, Litwin S, Cukierman E, and Klein-Szanto AJ (2005). PACE4 expression in mouse basal keratinocytes results in basement membrane disruption and acceleration of tumor progression. Cancer Res 65, 7310-7319.
36. Cheng M, Watson PH, Paterson JA, Seidah N, Chretien M, and Shiu RP (1997). Pro-protein convertase gene expression in human breast cancer. Int J Cancer 71, 966-971.
37. Ruggeri B, Caamano J, Slaga TJ, Conti CJ, Nelson WJ, and Klein-Szanto AJ (1992). Alterations in the expression of uvomorulin and Na+,K(+)-adenosine triphosphatase during mouse skin tumor progression. Am J Pathol 140, 1179-1185.
38. Lichti U, Anders J, and Yuspa SH (2008). Isolation and short-term culture of primary keratinocytes, hair follicle populations and dermal cells from newborn mice and keratinocytes from adult mice for in vitro analysis and for grafting to immunodeficient mice. Nat Protoc 3, 799-810.
39. Charpentier E, Lavker RM, Acquista E, and Cowin P (2000). Plakoglobin suppresses epithelial proliferation and hair growth in vivo. J Cell Biol 149, 503-520.
40. Fu J, Jin F, Zhang J, Fong K, Bassi DE, Lopez De Cicco R, Ramaraju D, Braunewell KH, Conti C, Benavides F, et al. (2010). VILIP-1 expression in vivo results in decreased mouse skin keratinocyte proliferation and tumor development. PLoS One 5, e10196.
41. Mahloogi H, Gonzalez-Guerrico AM, Lopez De Cicco R, Bassi DE, Goodrow T, Braunewell KH, and Klein-Szanto AJ (2003). Overexpression of the calcium sensor visinin-like protein-1 leads to a cAMP-mediated decrease of in vivo and in vitro growth and invasiveness of squamous cell carcinoma cells. Cancer Res 63, 4997-5004.
42. Lopez De Cicco R, Bassi DE, Page R, and Klein-Szanto AJ (2002). Furin expression in squamous cell carcinomas of the oral cavity and other sites evaluated by tissue microarray technology. Acta Odontol Latinoam 15, 29-37.
43. Page RE, Klein-Szanto AJ, Litwin S, Nicolas E, Al-Jumaily R, Alexander P, Godwin AK, Ross EA, Schilder RJ, and Bassi DE (2007). Increased expression of the pro-protein convertase furin predicts decreased survival in ovarian cancer. Cell Oncol 29, 289-299.
44. Bassi DE, Zhang J, Cenna J, Litwin S, Cukierman E, and Klein-Szanto AJ (2010). Proprotein convertase inhibition results in decreased skin cell proliferation, tumorigenesis, and metastasis. Neoplasia 12, 516-526.
45. Blanchette F, Day R, Dong W, Laprise MH, and Dubois CM (1997). TGFβ1 regulates gene expression of its own converting enzyme furin. J Clin Invest 99, 1974-1983.
46. Dubois CM, Blanchette F, Laprise MH, Leduc R, Grondin F, and Seidah NG (2001). Evidence that furin is an authentic transforming growth factor-β1-converting enzyme. Am J Pathol 158, 305-316.
47. Lopez De Cicco R, Watson JC, Bassi DE, Litwin S, and Klein-Szanto AJ (2004). Simultaneous expression of furin and vascular endothelial growth factor in human oral tongue squamous cell carcinoma progression. Clin Cancer Res 10, 4480-4488.
48. Lapouge G, Youssef KK, Vokaer B, Achouri Y, Michaux C, Sotiropoulou PA, and Blanpain C (2011). Identifying the cellular origin of squamous skin tumors. Proc Natl Acad Sci USA 108, 7431-7436.
49. Morris RJ, Tryson KA, and Wu KQ (2000). Evidence that the epidermal targets of carcinogen action are found in the interfollicular epidermis of infundibulum as well as in the hair follicles. Cancer Res 60, 226-229.
50. Hansen LA and Tennant RW (1994). Follicular origin of epidermal papillomas in v-Ha-ras transgenic TG.AC mouse skin. Proc Natl Acad Sci USA 91, 7822-7826.
51. Scopsi L, Gullo M, Rilke F, Martin S, and Steiner DF (1995). Proprotein convertases (PC1/PC3 and PC2) in normal and neoplastic human tissues: their use as markers of neuroendocrine differentiation. J Clin Endocrinol Metab 80, 294-301.