Skip to main content

Advertisement

SpringerLink
Log in

Decreased blood levels of B lymphocytes and NK cells in patients with systemic lupus erythematosus (SLE) infected with papillomavirus (HPV)

  • Original Paper
  • Published:
Archives of Dermatological Research Aims and scope Submit manuscript

Abstract

Patients with systemic lupus erythematosus (SLE) show an enhanced risk to develop human papillomavirus (HPV) infection, and aggressive forms of this condition are seen in these patients. The aim of this study was to assess the possible relationship among HPV infection, immunosuppressive therapy and levels of leukocyte subsets in patients with SLE. The following individuals were included in the study: (1) SLE patients under immunosuppressive therapy and with lesions caused by HPV (n = 16); (2) SLE patients under immunosuppressive therapy and no evidence of HPV infection (n = 20); (3) untreated SLE patients with no evidence of HPV infection (n = 7), and; (4) healthy female subjects without evidence of HPV infection (n = 10). Peripheral blood was obtained and the percentages of different lymphocyte subsets were determined by flow cytometry, with the use of the following monoclonal antibodies: CD3, CD4, CD8, CD16, CD19, CD20, CD22, CD56, and CD335 (NKp46). We found that SLE patients under immunosuppressive therapy and with lesions caused by HPV showed significantly lower levels of B lymphocytes and NK cells compared to other groups. In contrast, SLE patients receiving immunosuppressive drugs and with no evidence of HPV infection showed similar levels of B and NK cells than healthy controls. Those patients receiving mycophenolate mofetil (MMF) had a diminished number of B cells, and a positive correlation was detected between the dose of MMF and the number of HPV skin lesions. Our data suggest that therapy of SLE patients with MMF is associated with diminished levels of B and NK cells and an enhanced risk for HPV infection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Arens MJ, Wyllie AH, Bird CC (1990) Papillomaviruses and human cancer. Hum Pathol 21:686–698

    Article  Google Scholar 

  2. Barzegar C, Paul C, Saiag P, Cassenot P, Bachelez H, Autran B, Gorochov G, Petit A, Dubertret L (1998) Epidermodysplasia verruciformis-like eruption complicating human immunodeficiency virus infection. Br J Dermatol 139:122–127

    Article  PubMed  CAS  Google Scholar 

  3. Blumenfeld Z, Lorber M, Yofee N, Scharf Y (1994) Systemic lupus erythematosus: predisposition for uterine cervical dysplasia. Lupus 3:59–61

    Article  PubMed  CAS  Google Scholar 

  4. Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis studies in SLE. Arthr Rheum 35:630–640

    Article  CAS  Google Scholar 

  5. Bonagura VR, Hatam LJ, Rosenthal DW, de Voti JA, Lam F, Steinberg BM, Abramson AL (2010) Recurrent respiratory papillomatosis: a complex defect in immune responsiveness to human papillomavirus-6 and 11. APMIS 118:455–470

    Article  PubMed  CAS  Google Scholar 

  6. Cutts FT, Franceschi S, Goldie S, Castellsague X, de Sanjose S, Garnett G, Edmunds WJ, Claeys P, Goldenthal KL, Harper DM, Markowitz L (2007) Human papillomavirus and HPV vaccines: a review. Bull World Health Org 85:719–726

    Article  PubMed  CAS  Google Scholar 

  7. Cluffo G (1907) Innesto positive confiltrato di verruca volgare (positive verruca vulgaris inoculatium using a filtered inoculum). G Ital Mal Venereol 48:12–17

    Google Scholar 

  8. Dave R, Monk B, Mahaffey P (2002) Spontaneous disappearance of refractory viral warts at distant sites following carbon-dioxide laser treatment. Br J Plast Surg 55:696–698

    Article  PubMed  CAS  Google Scholar 

  9. Davey DD (2003) Cervical cytology classification and the Bethesda System. Cancer J 9:327–334

    Article  PubMed  Google Scholar 

  10. De Roy PG (2004) Helsinki and the Declaration of Helsinki. World Med J 50:9–11

    Google Scholar 

  11. Febronio MV, Pereira RM, Bonfa E, Takiuti AD, Pereyra EA, Silva CA (2007) Inflammatory cervicovaginal cytology is associated with disease activity in juvenile systemic lupus erythematosus. Lupus 16:430–435

    Article  PubMed  CAS  Google Scholar 

  12. Firnhaber C, Van Le H, Pettifor A, Schulze D, Michelow P, Sanne IM, Lewis DA, Williamson AL, Allan B, Williams S, Rinas A, Levin S, Smith JS (2010) Association between cervical dysplasia and human papillomavirus in HIV seropositive women from Johannesburg South Africa. Cancer Causes Control 21:433–443

    Article  PubMed  Google Scholar 

  13. Garzetti GG, Ciavattini A, Goteri G, Nictolis M, Menso S, Muzzioli M, Fabris N (1995) HPV DNA positivity and natural killer activity in the clinical outcome of mild cervical dysplasia: integration between virus and immune system. Gynecol Obstet Invest 39:130–135

    Article  PubMed  CAS  Google Scholar 

  14. Johansson E, Pyrhönen S, Rostila T (1977) Warts and wart virus in patients with systemic lupus erythematosus. Br Med J 1:74–76

    Article  PubMed  CAS  Google Scholar 

  15. Klumb EM, Pinto AC, Jesus GR, Araujo M Jr, Jascone L, Gayer CR, Ribeiro FM, Albuquerque EM, Macedo JM (2010) Are women with lupus at higher risk of HPV infection? Lupus 19:1485–1491

    Article  PubMed  CAS  Google Scholar 

  16. Korkmaz C, Ürer SM (2004) Cutaneous warts in patients with lupus erythematosus. Rheumatol Int 24:137–140

    Article  PubMed  Google Scholar 

  17. Kostaki M, Venetz JP, Nseir G, Meylan P, Sahli R, Pascual M, Laffitte E (2010) Giant warts in a kidney transplant patient: regression with sirolimus. Br J Dermatol 162:1148–1150

    Article  PubMed  CAS  Google Scholar 

  18. Kuijpers TW, Baars PA, Dantin C, van den Burg M, van Lier RA, Roosnek E (2008) Human NK cells can control CMV infection in the absence of T cells. Blood 112:914–915

    Article  PubMed  CAS  Google Scholar 

  19. Maeda K, Jimbow K, Fukushima M, Sawada Y, Fujinaga K (1985) Epidermodysplasia verruciformis associated with Bowen’s carcinoma, B lymphocytopenia and decreased immune functions. Dermatologica 171:478–485

    Article  PubMed  CAS  Google Scholar 

  20. Matteucci P, Magni M, Di Nicola M, Carlo-Stella C, Uberti C, Gianni AM (2002) Leukoencephalopathy and papovavirus infection after treatment with chemotherapy and anti-CD20 monoclonal antibody. Blood 100:1104–1105

    Article  PubMed  Google Scholar 

  21. Nebesio CL, Mirowsky GW, Chuang T (2001) Human papillomavirus: clinical significance and malignant potential. Int J Dermatol 40:373–379

    Article  PubMed  CAS  Google Scholar 

  22. Ohata K, Espinoza JL, Lu X, Kondo Y, Nakao S (2011) Mycophenolic acid inhibits natural killer proliferation and cytotoxic function: a possible disadvantage of including mycophenolate mofetil in the graft-versus-host disease prophylaxis regimen. Biol Blood Marrow Transplant 17:205–213

    Article  PubMed  CAS  Google Scholar 

  23. Ritter ML, Pirofski L (2009) Mycophenolate mofetil: effects on cellular immune subsets, infectious complications, and antimicrobial activity. Transpl Infect Dis 11:290–297

    Article  PubMed  CAS  Google Scholar 

  24. Santana IU, Gomes Ado N, Lyrio LD, Rios Grassi MF, Santiago MB (2011) Systemic lupus erythematosus, human papillomavirus infection, cervical pre-malignant and malignant lesions: a systematic review. Clin Rheumatol 30:665–672

    Article  PubMed  Google Scholar 

  25. Schiffman MH, Bauer HM, Hoover RN (1993) Epidemiologic evidence showing that human papillomavirus infection causes most cervical intraepithelial neoplasia. J Natl Cancer Inst 85:958–964

    Article  PubMed  CAS  Google Scholar 

  26. Schmook T, Nindl I, Ulrich C, Meyer T, Sterry W, Stockfleth E (2003) Viral warts in organ transplant recipients: new aspects in therapy. Br J Dermatol 149(Suppl 66):20–24

    Article  PubMed  Google Scholar 

  27. Scott M, Nakagawa M, Moscicki AB (2001) Cell-mediated immune response to human papillomavirus infection. Clin Diagn Lab Immunol 8:209–220

    PubMed  CAS  Google Scholar 

  28. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Regional Unit of Rheumatology and Osteoporosis, Hospital Central “Dr. Ignacio Morones Prieto”, School of Medicine, Universidad Autónoma de San Luis Potosí, San Luis Potosí, Mexico

    C. Abud-Mendoza, E. Cuevas-Orta, E. N. Santillán-Guerrero, M. U. Martínez-Martínez & L. Baranda

  2. Department of Immunology, School of Medicine, Universidad Autónoma de San Luis Potosí, Ave. V. Carranza 2405, 78210, San Luis Potosí, SLP, Mexico

    B. Hernández-Castro, L. Estrada-Capetillo, R. González-Amaro & L. Baranda

Authors
  1. C. Abud-Mendoza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Cuevas-Orta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. N. Santillán-Guerrero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. U. Martínez-Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. Hernández-Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. L. Estrada-Capetillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R. González-Amaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. L. Baranda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Baranda.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abud-Mendoza, C., Cuevas-Orta, E., Santillán-Guerrero, E.N. et al. Decreased blood levels of B lymphocytes and NK cells in patients with systemic lupus erythematosus (SLE) infected with papillomavirus (HPV). Arch Dermatol Res 305, 117–123 (2013). https://doi.org/10.1007/s00403-012-1258-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00403-012-1258-9

Keywords

Search

Navigation