Enhanced UV-induced skin carcinogenesis in transgenic mice overexpressing proprotein convertases

Neoplasia (United States)

Volumn 15, Issue 2, 2013, Pages 169-179

  Fu, Jian ^a   Bassi, Daniel E ^a   Zhang, Jirong ^a   Li, Tianyu ^a   Cai, Kathy Q ^a   Testa, Courtney Lyons ^a   Nicolas, Emmanuelle ^a   Klein Szanto, Andres J ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FURIN; SERINE PROTEINASE;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INCIDENCE; CANCER SUSCEPTIBILITY; CELL PROLIFERATION; CONTROLLED STUDY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN CARCINOGENESIS; SQUAMOUS CELL CARCINOMA; TRANSGENIC MOUSE; ULTRAVIOLET RADIATION; WESTERN BLOTTING;

EID: 84873506361     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.121846     Document Type: Article

References (63)

1. Yamagiwa K and Ishikawa K (1914). Ueber die atypische Epithelwucherung. Verhandl Jap Path Ges 4, 136.
2. Slaga TJ, DiGiovanni J, Winberg LD, and Budunova IV (1995). Skin carcinogenesis: characteristics, mechanisms, and prevention. Prog Clin Biol Res 391, 1-20.
3. DiGiovanni J (1992). Multistage carcinogenesis in mouse skin. Pharmacol Ther 54, 63-128.
4. Yuspa SH, Dlugosz AA, Denning MF, and Glick AB (1996). Multistage carcinogenesis in the skin. J Investig Dermatol Symp Proc 1, 147-150.
5. de Gruijl FR (2002). Photocarcinogenesis: UVA vs. UVB radiation. Skin Pharmacol Appl Skin Physiol 15, 316-320.
6. Seidah NG (2011). What lies ahead for the proprotein convertases? Ann N Y Acad Sci 1220, 149-161.
7. Seidah NG (2011). The proprotein convertases, 20 years later. Methods Mol Biol 768, 23-57.
8. Seidah NG and Prat A (2012). The biology and therapeutic targeting of the proprotein convertases. Nat Rev Drug Discov 11, 367-383.
9. 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.
10. 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.
11. 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.
12. Duguay SJ, Milewski WM, Young BD, Nakayama K, and Steiner DF (1997). Processing of wild-type and mutant proinsulin-like growth factor-IA by subtilisin-related proprotein convertases. J Biol Chem 272, 6663-6670.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. Komiyama T, Coppola JM, Larsen MJ, van Dort ME, Ross BD, Day R, Rehemtulla A, and Fuller RS (2009). Inhibition of furin/proprotein convertase-catalyzed surface and intracellular processing by small molecules. J Biol Chem 284, 15729-15738.
19. Yana I and Weiss SJ (2000). Regulation of membrane type-1 matrix metalloproteinase activation by proprotein convertases. Mol Biol Cell 11, 2387-2401.
20. Bergeron E, Basak A, Decroly E, and Seidah NG (2003). Processing of α4 integrin by the proprotein convertases: histidine at position P6 regulates cleavage. Biochem J 373, 475-484.
21. Mayer G, Boileau G, and Bendayan M (2003). Furin interacts with proMT1-MMP and integrin αV at specialized domains of renal cell plasma membrane. J Cell Sci 116, 1763-1773.
22. 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.
23. 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.
24. Lehmann M, Rigot V, Seidah NG, Marvaldi J, and Lissitzky JC (1996). Lack of integrin α-chain endoproteolytic cleavage in furin-deficient human colon adeno-carcinoma cells LoVo. Biochem J 317(pt 3), 803-809.
25. 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.
26. 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.
27. Artenstein AW and Opal SM (2011). Proprotein convertases in health and disease. N Engl J Med 365, 2507-2518.
28. 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.
29. Maret D, Sadr MS, Sadr ES, Colman DR, Del Maestro RF, and Seidah NG (2012). Opposite roles of furin and PC5A in N-cadherin processing. Neoplasia 14, 880-892.
30. Couture F, D'Anjou F, Desjardins R, Boudreau F, and Day R (2012). Role of proprotein convertases in prostate cancer progression. Neoplasia 14, 1032-1042.
31. Bassi DE, Lopez De Cicco R, Mahloogi H, Zucker S, Thomas G, and Klein-Szanto AJ (2001). Furin inhibition results in absent or decreased invasive-ness and tumorigenicity of human cancer cells. Proc Natl Acad Sci USA 98, 10326-10331.
32. 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.
33. 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.
34. 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.
35. De Vos L, Declercq J, Rosas GG, Van Damme B, Roebroek A, Vermorken F, Ceuppens J, van de Ven W, and Creemers J (2008). MMTV-cre-mediated fur inactivation concomitant with PLAG1 proto-oncogene activation delays salivary gland tumorigenesis in mice. Int J Oncol 32, 1073-1083.
36. Mahloogi H, Bassi DE, and Klein-Szanto AJ (2002). Malignant conversion of non-tumorigenic murine skin keratinocytes overexpressing PACE4. Carcino-genesis 23, 565-572.
37. Bassi DE, Fu J, Lopez de Cicco R, and Klein-Szanto AJ (2005). Proprotein convertases: master switches in the regulation of tumor growth and progression. Mol Carcinog 44, 151-161.
38. 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.
39. Rounseville MP and Davis TP (2000). Prohormone convertase and autocrine growth factor mRNAs are coexpressed in small cell lung carcinoma. J Mol Endocrinol 25, 121-128.
40. Hagiwara S, Murakumo Y, Mii S, Shigetomi T, Yamamoto N, Furue H, Ueda M, and Takahashi M (2010). Processing of CD109 by furin and its role in the regulation of TGF-β signaling. Oncogene 29, 2181-2191.
41. 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.
42. 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.
43. Fu J, Bassi DE, Zhang J, Li T, Nicolas E, and Klein-Szanto AJ (2012). Transgenic overexpression of the proprotein convertase furin enhances skin tumor growth. Neoplasia 14, 271-282.
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. Skiba B, Neill B, and Piva TJ (2005). Gene expression profiles of TNF-α, TACE, furin, IL-1β and matrilysin in UVA-and UVB-irradiated HaCat cells. Photodermatol Photoimmunol Photomed 21, 173-182.
46. Wilgus TA, Koki AT, Zweifel BS, Kusewitt DF, Rubal PA, and Oberyszyn TM (2003). Inhibition of cutaneous ultraviolet light B-mediated inflammation and tumor formation with topical celecoxib treatment. Mol Carcinog 38, 49-58.
47. Cooper SJ, MacGowan J, Ranger-Moore J, Young MR, Colburn NH, and Bowden GT (2003). Expression of dominant negative c-jun inhibits ultraviolet B-induced squamous cell carcinoma number and size in an SKH-1 hairless mouse model. Mol Cancer Res 1, 848-854.
48. Beissert S, Bluestone JA, Mindt I, Voskort M, Metze D, Mehling A, Luger TA, Schwarz T, and Grabbe S (1999). Reduced ultraviolet-induced carcinogenesis in mice with a functional disruption in B7-mediated costimulation. J Immunol 163, 6725-6731.
49. +-adenosine triphosphatase during mouse skin tumor progression. Am J Pathol 140, 1179-1185.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. 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.
57. 86 by members of the proprotein convertase family is functionally correlated to platelet-derived growth factor-A-induced functions and tumorigenicity. Cancer Res 63, 1458-1463.
58. 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.
59. Bassi DE and Klein-Szanto AJ (2007). Carcinogen-induced animal models of head and neck squamous cell carcinoma. Curr Protoc Pharmacol Chapter 14, Unit 14.2.
60. Walaszek Z, Hanausek M, and Slaga TJ (2007). The role of skin painting in predicting lung cancer. Int J Toxicol 26, 345-351.
61. Scamuffa N, Calvo F, Chretien M, Seidah NG, and Khatib AM (2006). Pro-protein convertases: lessons from knockouts. FASEB J 20, 1954-1963.
62. Steinel HH and Baker RS (1988). Sensitivity of HRA/Skh hairless mice to initiation/promotion of skin tumors by chemical treatment. Cancer Lett 41, 63-68.
63. Strickland PT and Swartz RP (1987). Inheritance of susceptibility to photo-tumorigenesis and persistent hyperplasia in F1 hybrids between SENCAR mice and BALB/c or C57BL/6 mice. Cancer Res 47, 6294-6296.