Defensins induce the recruitment of dendritic cells in cervical human papillomavirus-associated (pre)neoplastic lesions formed in vitro and transplanted in vivo

FASEB Journal

Volumn 21, Issue 11, 2007, Pages 2765-2775

  Hubert, Pascale ^a,d   Herman, Ludivine ^a   Maillard, Catherine ^b   Caberg, Jean Hubert ^a   Nikkels, Arjen ^c   Pierard, Gerald ^c   Foidart, Jean Marie ^b   Noel, Agnès ^b   Boniver, Jacques ^a   Delvenne, Philippe ^a  

^a Department of Pathology ^*

^b Laboratory of Tumor and Development Biology

^c UNIVERSITY OF LIÈGE   (Belgium)

^d UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Alpha and beta defensins; Antigen presenting cells; Cervical lesions; HPV; Migration

Indexed keywords

ALPHA DEFENSIN; BETA DEFENSIN; DEFENSIN; MESSENGER RNA;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INVASION; CELL CULTURE; CELL INFILTRATION; CELL MIGRATION; CELL TRANSPLANTATION; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOLOGY; IN VITRO STUDY; IN VIVO STUDY; KERATINOCYTE; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UTERINE CERVIX; UTERINE CERVIX CANCER; WART VIRUS;

ALPHA-DEFENSINS; ANIMALS; BETA-DEFENSINS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TRANSFORMED; CELL MOVEMENT; CERVICAL INTRAEPITHELIAL NEOPLASIA; CERVIX UTERI; DENDRITIC CELLS; EPITHELIUM; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; KERATINOCYTES; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM INVASIVENESS; ORGAN CULTURE TECHNIQUES; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PRECANCEROUS CONDITIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED; UTERINE CERVICAL NEOPLASMS;

HUMAN PAPILLOMAVIRUS; MUS;

EID: 34548476495     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7646com     Document Type: Article

References (51)

1. Bosch, F. X., and Munoz, N. (2002) The viral etiology of cervical cancer. Virus Res. 89, 183-190
2. Al-Saleh, W., Giannini, S. L., Jacobs, N., Moutchen, M., Doyen, J., Boniver, J., and Delvenne, P. (1998) Correlation of T-helper secretory differentiation and types of antigen-presenting cells in squamous intraepithelial lesions of the uterine cervix. J. Pathol. 184, 283-290
3. Calore, E. E., Cavaliere, M. J., Perez Calore, N. M., de Souza Dias, S., Paes Dos Santos, R., and Vilela-De-Almeida, L. (2001) Expression of Ki-67 in cervical epithelial cells in preneoplastic lesions of patients with AIDS. Gynecol. Obstet. Invest. 51, 51-54
4. Thivolet, J., Viac, J., and Staquet, M. J. (1982) Cell-mediated immunity in wart infection. Int. J. Dermatol. 21, 94-98
5. Hughes, R. G., Norval, M., and Howie, S. E. (1988) Expression of major histocompatibility class II antigens by Langerhans' cells in cervical intraepithelial neoplasia. J. Clin. Pathol. 41, 253-259
6. Memar, O. M., Arany, I., and Tyring, S. K. (1995) Skin-associated lymphoid tissue in human immunodeficiency virus-1, human papillomavirus, and herpes simplex virus infections. J. Invest Dermatol. 105, 99S-104S
7. Giannini, S. L., Hubert, P., Doyen, J., Boniver, J., and Delvenne, P. (2002) Influence of the mucosal epithelium microenvironment on Langerhans cells: implications for the development of squamous intraepithelial lesions of the cervix. Int. J. Cancer. 97, 654-659
8. Hubert, P., Greimers, R., Franzen-Detrooz, E., Doyen, J., Delanoye, P., Boniver, J., and Delvenne, P. (1998) In vitro propagated dendritic cells from patients with human-papilloma virus-associated preneoplastic lesions of the uterine cervix: use of Flt3 ligand. Cancer Immunol. Immunother. 47, 81-89
9. Charbonnier, A. S., Kohrgruber, N., Kriehuber, E., Stingl, G., Rot, A., and Maurer, D. (1999) Macrophage inflammatory protein 3alpha is involved in the constitutive trafficking of epidermal langerhans cells. J. Exp. Med. 190, 1755-1768
10. Yang, D., Chertov, O., Bykovskaia, S. N., Chen, Q., Buffo, M. J., Shogan, J., Anderson, M., Schroder, J. M., Wang, J. M., Howard, O. M., et al. (1999) Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286, 525-528
11. Mallow, E. B., Harris, A., Salzman, N., Russell, J. P., DeBerardinis, R. J., Ruchelli, E., and Bevins, C. L. (1996) Human enteric defensins. Gene structure and developmental expression. J. Biol. Chem. 271, 4038-4045
12. Agerberth, B., Charo, J., Werr, J., Olsson, B., Idali, F., Lindbom, L., Kiessling, R., Jornvall, H., Wigzell, H., and Gudmundsson, G. H. (2000) The human antimicrobial and chemotactic peptides LL-37 and alpha-defensins are expressed by specific lymphocyte and monocyte populations. Blood. 96, 3086-3093
13. Chen, H., Xu, Z., Peng, L., Fang, X., Yin, X., Xu, N., and Cen, P. (2006) Recent advances in the research and development of human defensins. Peptides. 27, 931-940
14. Sorensen, O. E., Thapa, D. R., Rosenthal, A., Liu, L., Roberts, A. A., and Ganz, T. (2005) Differential regulation of beta-defensin expression in human skin by microbial stimuli. J. Immunol. 174, 4870-4879
15. Yang, D., Chen, Q., Chertov, O., and Oppenheim, J. J. (2000) Human neutrophil defensins selectively chemoattract naive T and immature dendritic cells. J. Leukoc. Biol. 68, 9-14
16. Delvenne, P., Al-Saleh, W., Gilles, C., Thiry, A., and Boniver, J. (1995) Inhibition of growth of normal and human papillomavirus-transformed keratinocytes in monolayer and organotypic cultures by interferon-G and tumor necrosis factor-A. Am. J. Pathol. 146, 589-598
17. 2+-dependent mechanism. J. Exp. Med. 186, 467-472
18. Bajou, K., Noel, A., Gerard, R. D., Masson, V., Brunner, N., Holst-Hansen, C., Skobe, M., Fusenig, N. E., Carmeliet, P., Collen, D., et al. (1998) Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nat. Med. 4, 923-928
19. Hubert, P., Van Den Brule, F., Giannini, S. L., Franzen-Detrooz, E., Boniver, J., and Delvenne, P. (1999) Colonization of in vitro-formed cervical human papillomavirus-associated (pre) neoplastic lesions with dendritic cells. Role of granulocyte/macrophage colony-stimulating factor. Am. J. Pathol. 154, 775-784
20. Pater, M. M., and Pater, A. (1985) Human papillomavirus types 16 and 18 sequences in carcinoma cell lines of the cervix. Virology. 145, 313-318
21. Friedl, F., Kimura, I., Osato, T., and Ito, Y. (1970) Studies on a new human cell line (SiHa) derived from carcinoma of uterus. I. Its establishment and morphology. Proc. Soc. Exp. Biol. 135, 543-545
22. Renard, I., Mezzanzanica, D., Canevari, S., Ferrini, S., Boniver, J., Delvenne, P., and Jacobs, N. (2002) Anti-CD3/anti-epidermal growth factor receptor-bispecific antibody retargeting of lymphocytes against human neoplastic keratinocytes in an autologous organotypic culture model. Am. J. Pathol. 160, 113-122
23. Hubert, P., Caberg, J. H., Gilles, C., Bousarghin, L., Franzen-Detrooz, E., Boniver, J., and Delvenne, P. (2005) E-cadherin-dependent adhesion of dendritic and Langerhans cells to keratinocytes is defective in cervical human papillomavirus-associated (pre)neoplastic lesions. J. Pathol. 206, 346-355
24. Hubert, P., Giannini, S. L., Vanderplasschen, A., Franzen-Detrooz, E., Jacobs, N., Boniver, J., and Delvenne, P. (2001) Dendritic cells induce the death of human papillomavirus-transformed keratinocytes1. FASEB J. 15, 2521-2523
25. Hubert, P., Bousarghin, L., Greimers, R., Franzen-Detrooz, E., Boniver, J., and Delvenne, P. (2005) Production of large numbers of Langerhans' cells with intraepithelial migration ability in vitro. Exp. Dermatol. 14, 469-477
26. Chadebech, P., Goidin, D., Jacquet, C., Viac, J., Schmitt, D., and Staquet, M. J. (2003) Use of human reconstructed epidermis to analyze the regulation of beta-defensin hBD-1, hBD-2, and hBD-3 expression in response to LPS. Cell Biol. Toxicol. 19, 313-324
27. Duits, L. A., Ravensbergen, B., Rademaker, M., Hiemstra, P. S., and Nibbering, P. H. (2002) Expression of beta-defensin 1 and 2 mRNA by human monocytes, macrophages and dendritic cells. Immunology. 106, 517-525
28. Andrade, W., Seabrook, T. J., Johnston, M. G., and Hay, J. B. (1996) The use of the lipophilic fluorochrome CM-DiI for tracking the migration of lymphocytes. J. Immunol. Methods 194, 181-189
29. Chertov, O., Michiel, D. F., Xu, L., Wang, J. M., Tani, K., Murphy, W. J., Longo, D. L., Taub, D. D., and Oppenheim, J. J. (1996) Identification of defensin-1, defensin-2, and CAP37/azurocidin as T-cell chemoattractant proteins released from interleukin-8-stimulated neutrophils. J. Biol. Chem. 271, 2935-2940
30. Noel, A., Maillard, C., Rocks, N., Jost, M., Chabottaux, V., Sounni, N. E., Maquoi, E., Cataldo, D., and Foidart, J. M. (2004) Membrane-associated proteases and their inhibitors in tumour angiogenesis. J. Clin. Pathol. 57, 577-584
31. Weinberg, A., Quinones-Mateu, M. E., and Lederman, M. M. (2006) Role of human beta-defensins in HIV infection. Adv. Dent. Res. 19, 42-48
32. Wang, W., Owen, S. M., Rudolph, D. L., Cole, A. M., Hong, T., Waring, A. J., Lal, R. B., and Lehrer, R. I. (2004) Activity of alpha- and theta-defensins against primary isolates of HIV-1. J. Immunol. 173, 515-520
33. Buck, C. B., Day, P. M., Thompson, C. D., Lubkowski, J., Lu, W., Lowy, D. R., and Schiller, J. T. (2006) Human alpha-defensins block papillomavirus infection. Proc. Natl. Acad. Sci. U. S. A. 103, 1516-1521
34. Papo, N., and Shai, Y. (2005) Host defense peptides as new weapons in cancer treatment. Cell Mol. Life. Sci. 62, 784-790
35. McKeown, S. T., Lundy, F. T., Nelson, J., Lockhart, D., Irwin, C. R., Cowan, C. G., and Marley, J. J. (2006) The cytotoxic effects of human neutrophil peptide-1 (HNP1) and lactoferrin on oral squamous cell carcinoma (OSCC) in vitro. Oral Oncol 42, 685-690
36. Kaplan, G., Walsh, G., Guido, L. S., Meyn, P., Burkhardt, R. A., Abalos, R. M., Barker, J., Frindt, P. A., Fajardo, T. T., and Celona, R. (1992) Novel responses of human skin to intradermal recombinant granulocyte/macrophage- colony-stimulating factor: Langerhans cell recruitment, keratinocyte growth, and enhanced wound healing. J. Exp. Med. 175, 1717-1728
37. Havard, L., Rahmouni, S., Boniver, J., and Delvenne, P. (2005) High levels of p105 (NFKB1) and p100 (NFKB2) proteins in HPV16-transformed keratinocytes: role of E6 and E7 oncoproteins. Virology 331, 357-366
38. Ali, R. S., Falconer, A., Ikram, M., Bissett, C. E., Cerio, R., and Quinn, A. G. (2001) Expression of the peptide antibiotics human beta defensin-1 and human beta defensin-2 in normal human skin. J. Invest. Dermatol. 117, 106-111
39. Howell, M. D., Novak, N., Bieber, T., Pastore, S., Girolomoni, G., Boguniewicz, M., Streib, J., Wong, C., Gallo, R. L., and Leung, D. Y. (2005) Interleukin-10 downregulates anti-microbial peptide expression in atopic dermatitis. J. Invest. Dermatol. 125, 738-745
40. Giannini, S. L., Al-Saleh, W., Piron, H., Jacobs, N., Doyen, J., Boniver, J., and Delvenne, P. (1998) Cytokine expression in sqamous intraepithelial lesions of the uterine cervix: implications for the generation of local immunosuppression. Clin. Exp. Immunol. 113, 183-189
41. Masson, V., de la Ballina, L. R., Munaut, C., Wielockx, B., Jost, M., Maillard, C., Blacher, S., Bajou, K., Itoh, T., Itohara, S., et al. (2005) Contribution of host MMP-2 and MMP-9 to promote tumor vascularization and invasion of malignant keratinocytes. FASEB J. 19, 234-236
42. Matthews, K., Leong, C. M., Baxter, L., Inglis, E., Yun, K., Backstrom, B. T., Doorbar, J., and Hibma, M. (2003) Depletion of Langerhans cells in human papillomavirus type 16-infected skin is associated with E6-mediated down regulation of E-cadherin. J. Virol. 77, 8378-8385
43. Grutkoski, P. S., Graeber, C. T., Lim, Y. P., Ayala, A., and Simms, H. H. (2003) Alpha-defensin 1 (human neutrophil protein 1) as an antichemotactic agent for human polymorphonuclear leukocytes. Antimicrob. Agents. Chemother. 47, 2666-2668
44. Van Wetering, S., Mannesse-Lazeroms, S. P., van Sterkenburg, M. A., and Hiemstra, P. S. (2002) Neutrophil defensins stimulate the release of cytokines by airway epithelial cells: modulation by dexamethasone. Inflamm. Res. 51, 8-15
45. Lundy, F. T., Orr, D. F., Gallagher, J. R., Maxwell, P., Shaw, C., Napier, S. S., Gerald Cowan, C., Lamey, P. J., and Marley, J. J. (2004) Identification and overexpression of human neutrophil alpha-defensins (human neutrophil peptides 1, 2 and 3) in squamous cell carcinomas of the human tongue. Oral. Oncol. 40, 139-144
46. Mizukawa, N., Sugiyama, K., Kamio, M., Yamachika, E., Ueno, T., Fukunaga, J., Takagi, S., and Sugahara, T. (2000) Immunohistochemical staining of human alpha-defensin-1 (HNP-1), in the submandibular glands of patients with oral carcinomas. Anticancer. Res. 20, 1125-1127
47. Lillard, J. W. J., Boyaka, P. N., Chertov, O., Oppenheim, J. J., and McGhee, J. R. (1999) Mechanisms for induction of acquired host immunity by neutrophil peptide defensins. Proc. Natl. Acad. Sci. U. S. A. 96, 651-656
48. Conejo-Garcia, J. R., Benencia, F., Courreges, M. C., Kang, E., Mohamed-Hadley, A., Buckanovich, R. J., Holtz, D. O., Jenkins, A., Na, H., Zhang, L., et al. (2004) Tumor-infiltrating dendritic cell precursors recruited by a beta-defensin contribute to vasculogenesis under the influence of Vegf-A. Nat. Med. 10, 950 -958
49. Chavakis, T., Cines, D. B., Rhee, J. S., Liang, O. D., Schubert, U., Hammes, H. P., Higazi, A. A., Nawroth, P. P., Preissner, K. T., and Bdeir, K. (2004) Regulation of neovascularization by human neutrophil peptides (alpha-defensins): a link between inflammation and angiogenesis. FASEB J. 18, 1306-1308
50. Economopoulou, M., Bdeir, K., Cines, D. B., Fogt, F., Bdeir, Y., Lubkowski, J., Lu, W., Preissner, K. T., Hammes, H. P., and Chavakis, T. (2005) Inhibition of pathologic retinal neovascularization by alpha-defensins. Blood. 106, 3831-3838
51. Muller, C. A., Markovic-Lipkovski, J., Klatt, T., Gamper, J., Schwarz, G., Beck, H., Deeg, M., Kalbacher, H., Widmann, S., Wessels, J. T., et al. (2002) Human alpha-defensins HNPs-1, -2, and -3 in renal cell carcinoma: influences on tumor cell proliferation. Am. J. Pathol. 160, 1311-1324