Passive immunoprotection targeting a secreted CAMP factor of Propionibacterium acnes as a novel immunotherapeutic for acne vulgaris

Vaccine

Volumn 29, Issue 17, 2011, Pages 3230-3238

  Liu, Pei Feng ^a,b,c   Nakatsuji, Teruaki ^a,b   Zhu, Wenhong ^c   Gallo, Richard L ^a,b   Huang, Chun Ming ^a,b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c BURNHAM INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Acne vulgaris; Agroinfiltration; Passive immunization; Propionibacterium acnes; Radish leaves

Indexed keywords

CAMP FACTOR; IMMUNOMODULATING AGENT; MACROPHAGE INFLAMMATORY PROTEIN 2; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ACNE VULGARIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; COMMENSALISM; CONTROLLED STUDY; DRUG TARGETING; ENCAPSULATION; FEMALE; IMMUNITY; IMMUNOTHERAPY; MICROBIOME; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PASSIVE IMMUNIZATION; PLANT LEAF; PRIORITY JOURNAL; PROPIONIBACTERIUM ACNES; RADISH;

ACNE VULGARIS; ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, NEUTRALIZING; BACTERIAL LOAD; BACTERIAL PROTEINS; FEMALE; IMMUNIZATION, PASSIVE; IMMUNOTHERAPY; MICE; MICE, INBRED ICR; PROPIONIBACTERIUM ACNES; VIRULENCE FACTORS;

EID: 79954593764     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.02.036     Document Type: Article

References (73)

1. Gao Z., Tseng C.H., Pei Z., Blaser M.J. Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci USA 2007, 104(8):2927-2932.
2. Dekio I., Sakamoto M., Hayashi H., Amagai M., Suematsu M., Benno Y. Characterization of skin microbiota in patients with atopic dermatitis and in normal subjects using 16S rRNA gene-based comprehensive analysis. J Med Microbiol 2007, 56(Pt 12):1675-1683.
3. Brook I., Frazier E.H. Infections caused by Propionibacterium species. Rev Infect Dis 1991, 13(5):819-822.
4. Ahn C.Y., Ko C.Y., Wagar E.A., Wong R.S., Shaw W.W. Microbial evaluation: 139 implants removed from symptomatic patients. Plast Reconstr Surg 1996, 98(7):1225-1229.
5. Tancrede C. Role of human microflora in health and disease. Eur J Clin Microbiol Infect Dis 1992, 11(11):1012-1015.
6. Leyden J.J., McGinley K.J., Vowels B. Propionibacterium acnes colonization in acne and nonacne. Dermatology 1998, 196(1):55-58.
7. McGinley K.J., Webster G.F., Leyden J.J. Regional variations of cutaneous propionibacteria. Appl Environ Microbiol 1978, 35(1):62-66.
8. Grice E.A., Kong H.H., Conlan S., Deming C.B., Davis J., Young A.C., et al. Topographical and temporal diversity of the human skin microbiome. Science 2009, 324(5931):1190-1192.
9. Nishiwaki T., Yoneyama H., Eishi Y., Matsuo N., Tatsumi K., Kimura H., et al. Indigenous pulmonary Propionibacterium acnes primes the host in the development of sarcoid-like pulmonary granulomatosis in mice. Am J Pathol 2004, 165(2):631-639.
10. Yamada T., Eishi Y., Ikeda S., Ishige I., Suzuki T., Takemura T., et al. In situ localization of Propionibacterium acnes DNA in lymph nodes from sarcoidosis patients by signal amplification with catalysed reporter deposition. J Pathol 2002, 198(4):541-547.
11. Williams R.E., Doherty V.R., Perkins W., Aitchison T.C., Mackie R.M. Staphylococcus aureus and intra-nasal mupirocin in patients receiving isotretinoin for acne. Br J Dermatol 1992, 126(4):362-366.
12. Nakatsuji T., Liu Y.T., Huang C.P., Zoubouis C.C., Gallo R.L., Huang C.M. Antibodies elicited by inactivated Propionibacterium acnes-based vaccines exert protective immunity and attenuate the IL-8 production in human sebocytes: relevance to therapy for acne vulgaris. J Invest Dermatol 2008, 128(10):2451-2457.
13. Bruggemann H., Henne A., Hoster F., Liesegang H., Wiezer A., Strittmatter A., et al. The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 2004, 305(5684):671-673.
14. Kim J. Acne vaccines: therapeutic option for the treatment of acne vulgaris?. J Invest Dermatol 2008, 128(10):2353-2354.
15. Toyoda M., Morohashi M. Pathogenesis of acne. Med Electron Microsc 2001, 34(1):29-40.
16. Nakatsuji T., Rasochova L., Huang C.M. Vaccine therapy for P. acnes-associated diseases. Infect Disord Drug Targets 2008, 8(3):160-165.
17. Zouboulis C.C. Acne sebaceous gland function. Clin Dermatol 2004, 22(5):360-366.
18. Bruggemann H. Insights in the pathogenic potential of Propionibacterium acnes from its complete genome. Semin Cutan Med Surg 2005, 24(2):67-72.
19. Jurgens D., Sterzik B., Fehrenbach F.J. Unspecific binding of group B streptococcal cocytolysin (CAMP factor) to immunoglobulins and its possible role in pathogenicity. J Exp Med 1987, 165(3):720-732.
20. Lang S., Palmer M. Characterization of Streptococcus agalactiae CAMP factor as a pore-forming toxin. J Biol Chem 2003, 278(40):38167-38173.
21. Choudhury T.K. Synergistic lysis of erythrocytes by Propionibacterium acnes. J Clin Microbiol 1978, 8(2):238-241.
22. Christie R., Atkins N.E., Munch-Petersen E. A note on a lytic phenomenon shown by group B streptococci. Aust J Exp Biol Med Sci 1944, 22:197-200.
23. Lo C.W., Lai Y.K., Liu Y.T., Gallo R.L., Huang C.M. Staphylococcus aureus hijacks a skin commensal to intensify its virulence: immunization targeting beta-hemolysin and CAMP factor. J Invest Dermatol 2011, 131(2):401-409.
24. Ochsendorf F. Systemic antibiotic therapy of acne vulgaris. J Dtsch Dermatol Ges 2006, 4(10):828-841.
25. Slaga T.J., Klein-Szanto A.J., Triplett L.L., Yotti L.P., Trosko K.E. Skin tumor-promoting activity of benzoyl peroxide, a widely used free radical-generating compound. Science 1981, 213(4511):1023-1025.
26. Weinberg J.M. The utility of benzoyl peroxide in hydrophase base (Brevoxyl) in the treatment of acne vulgaris. J Drugs Dermatol 2006, 5(4):344-349.
27. Tanghetti E.A., Popp K.F. A current review of topical benzoyl peroxide: new perspectives on formulation and utilization. Dermatol Clin 2009, 27(1):17-24.
28. Zhao J., Lahiri-Chatterjee M., Sharma Y., Agarwal R. Inhibitory effect of a flavonoid antioxidant silymarin on benzoyl peroxide-induced tumor promotion, oxidative stress and inflammatory responses in SENCAR mouse skin. Carcinogenesis 2000, 21(4):811-816.
29. Simpson L.S., Burdine L., Dutta A.K., Feranchak A.P., Kodadek T. Selective toxin sequestrants for the treatment of bacterial infections. J Am Chem Soc 2009, 131(16):5760-5762.
30. Layton A.M., Dreno B., Gollnick H.P., Zouboulis C.C. A review of the European directive for prescribing systemic isotretinoin for acne vulgaris. J Eur Acad Dermatol Venereol 2006, 20(7):773-776.
31. Haider A., Shaw J.C. Treatment of acne vulgaris. JAMA 2004, 292(6):726-735.
32. McGinley K.J., Webster G.F., Leyden J.J. Facial follicular porphyrin fluorescence: correlation with age and density of Propionibacterium acnes. Br J Dermatol 1980, 102(4):437-441.
33. Mourelatos K., Eady E.A., Cunliffe W.J., Clark S.M., Cove J.H. Temporal changes in sebum excretion and propionibacterial colonization in preadolescent children with and without acne. Br J Dermatol 2007, 156(1):22-31.
34. Perry A.L., Lambert P.A. Propionibacterium acnes. Lett Appl Microbiol 2006, 42(3):185-188.
35. Nakatsuji T., Liu Y.T., Huang C.P., Zouboulis C.C., Gallo R.L., Huang C.M. Vaccination targeting a surface sialidase of P. acnes: implication for new treatment of acne vulgaris. PLoS One 2008, 3(2):e1551.
36. Rasko D.A., Moreira C.G., Li de R., Reading N.C., Ritchie J.M., Waldor M.K., et al. Targeting QseC signaling and virulence for antibiotic development. Science 2008, 321(5892):1078-1080.
37. Cogen A.L., Nizet V., Gallo R.L. Skin microbiota: a source of disease or defence?. Br J Dermatol 2008, 158(3):442-455.
38. Ma J.K. Genes, greens, and vaccines. Nat Biotechnol 2000, 18(11):1141-1142.
39. Tregoning J., Maliga P., Dougan G., Nixon P.J. New advances in the production of edible plant vaccines: chloroplast expression of a tetanus vaccine antigen, TetC. Phytochemistry 2004, 65(8):989-994.
40. Chargelegue D., Obregon P., Drake P.M. Transgenic plants for vaccine production: expectations and limitations. Trends Plant Sci 2001, 6(11):495-496.
41. Streatfield S.J., Jilka J.M., Hood E.E., Turner D.D., Bailey M.R., Mayor J.M., et al. Plant-based vaccines: unique advantages. Vaccine 2001, 19(17-19):2742-2748.
42. Shih S.M., Doran P.M. Foreign protein production using plant cell and organ cultures: advantages and limitations. Biotechnol Adv 2009, 27(6):1036-1042.
43. Soderquist B., Holmberg A., Unemo M. Propionibacterium acnes as an etiological agent of arthroplastic and osteosynthetic infections-two cases with specific clinical presentation including formation of draining fistulae. Anaerobe 2010, 16(3):304-306.
44. Jefferson R.A. Assaying chimeric genes in plants: the GUS gene fusion. Plant Mol Biol Rep 1987, 5(4):387-405.
45. Liu Y.T., Lin S.B., Huang C.P., Huang C.M. A novel immunogenic spore coat-associated protein in Bacillus anthracis: characterization via proteomics approaches and a vector-based vaccine system. Protein Expr Purif 2008, 57(1):72-80.
46. Liu P.F., Shi W., Zhu W., Smith J.W., Hsieh S.L., Gallo R.L., et al. Vaccination targeting surface FomA of Fusobacterium nucleatum against bacterial co-aggregation: implication for treatment of periodontal infection and halitosis. Vaccine 2010, 28(19):3496-3505.
47. An G., Ebert P.R., Mitra A., Ha S.B. Binary vectors. Plant molecular biology manual 1988, 1-19. Kluwer Academic Press;, Dordrecht. S.B. Gelvin, R.A. Schilperoort, D.P.S. Verma (Eds.).
48. Schob H., Kunz C., Meins F. Silencing of transgenes introduced into leaves by agroinfiltration: a simple, rapid method for investigating sequence requirements for gene silencing. Mol Gen Genet 1997, 256(5):581-585.
49. Mantis N.J. Vaccines against the category B toxins: Staphylococcal enterotoxin B, epsilon toxin and ricin. Adv Drug Deliv Rev 2005, 57(9):1424-1439.
50. Medina-Bolivar F., Wright R., Funk V., Sentz D., Barroso L., Wilkins T.D., et al. A non-toxic lectin for antigen delivery of plant-based mucosal vaccines. Vaccine 2003, 21(9-10):997-1005.
51. Davis S.S. Nasal vaccines. Adv Drug Deliv Rev 2001, 51(1-3):21-42.
52. Gil F., Titarenko E., Terrada E., Arcalis E., Escribano J.M. Successful oral prime-immunization with VP60 from rabbit haemorrhagic disease virus produced in transgenic plants using different fusion strategies. Plant Biotechnol J 2006, 4(1):135-143.
53. Liu P.F., Haake S.K., Gallo R.L., Huang C.M. A novel vaccine targeting Fusobacterium nucleatum against abscesses and halitosis. Vaccine 2009, 27(10):1589-1595.
54. Kim J. Review of the innate immune response in acne vulgaris: activation of toll-like receptor 2 in acne triggers inflammatory cytokine responses. Dermatology 2005, 211(3):193-198.
55. Kim J., Ochoa M.T., Krutzik S.R., Takeuchi O., Uematsu S., Legaspi A.J., et al. Activation of toll-like receptor 2 in acne triggers inflammatory cytokine responses. J Immunol 2002, 169(3):1535-1541.
56. Nagy I., Pivarcsi A., Kis K., Koreck A., Bodai L., McDowell A., et al. Propionibacterium acnes and lipopolysaccharide induce the expression of antimicrobial peptides and proinflammatory cytokines/chemokines in human sebocytes. Microbes Infect 2006, 8(8):2195-2205.
57. Itakura M., Tokuda A., Kimura H., Nagai S., Yoneyama H., Onai N., et al. Blockade of secondary lymphoid tissue chemokine exacerbates Propionibacterium acnes-induced acute lung inflammation. J Immunol 2001, 166(3):2071-2079.
58. Valanne S., McDowell A., Ramage G., Tunney M.M., Einarsson G.G., O'Hagan S., et al. CAMP factor homologues in Propionibacterium acnes: a new protein family differentially expressed by types I and II. Microbiology 2005, 151(Pt 5):1369-1379.
59. Holland C., Mak T.N., Zimny-Arndt U., Schmid M., Meyer T.F., Jungblut P.R., et al. Proteomic identification of secreted proteins of Propionibacterium acnes. BMC Microbiol 2010, 10:230.
60. Webster G.F., Ruggieri M.R., McGinley K.J. Correlation of Propionibacterium acnes populations with the presence of triglycerides on nonhuman skin. Appl Environ Microbiol 1981, 41(5):1269-1270.
61. Nakano K., Kiyokane K., Benvenuto-Andrade C., Gonzalez S. Real-timereflectance confocal microscopy, a noninvasive tool for in vivo quantitative evaluation of comedolysis in the rhino mouse model. Skin Pharmacol Physiol 2007, 20(1):29-36.
62. Takaoki M., Kawaji H. Impaired antibody response against T-dependent antigens in rhino mice. Immunology 1980, 40(1):27-32.
63. Semel J., Bowe B., Guo A., Lee L., Rife L., Polikoff D., et al. Propionibacterium acnes-enhanced lens-induced granulomatous uveitis in the rat. Invest Ophthalmol Vis Sci 1992, 33(5):1766-1770.
64. Kligman A.M. An overview of acne. J Invest Dermatol 1974, 62(3):268-287.
65. Chen Y.L., Yu C.K., Lei H.Y. Propionibacterium acnes induces acute TNFalpha-mediated apoptosis of hepatocytes followed by inflammatory T-cell-mediated granulomatous hepatitis in mice. J Biomed Sci 1999, 6(5):349-356.
66. Fletcher S.P., Muto M., Mayfield S.P. Optimization of recombinant protein expression in the chloroplasts of green algae. Adv Exp Med Biol 2007, 616:90-98.
67. Jabeen R., Khan M.S., Zafar Y., Anjum T. Codon optimization of cry1Ab gene for hyper expression in plant organelles. Mol Biol Rep 2010, 37(2):1011-1017.
68. Zhang J., Shi Z., Kong F.K., Jex E., Huang Z., Watt J.M., et al. Topical application of Escherichia coli-vectored vaccine as a simple method for eliciting protective immunity. Infect Immun 2006, 74(6):3607-3617.
69. Sendi P., Locher R., Bucheli B., Battegay M. Intranasal influenza vaccine in a working population. Clin Infect Dis 2004, 38(7):974-980.
70. A Keller M., Stiehm E.R. Passive immunity in prevention and treatment of infectious diseases. Clin Microbiol Rev 2000, 13(4):602-614.
71. Hu W.G., Nagata L.P. Antibody gene-based prophylaxis and therapy for biodefence. Hum Vaccin 2008, 4(1):74-78.
72. Casadevall A. Passive antibody administration (immediate immunity) as a specific defense against biological weapons. Emerg Infect Dis 2002, 8(8):833-841.
73. Li G., Badkar A., Nema S., Kolli C.S., Banga A.K. In vitro transdermal delivery of therapeutic antibodies using maltose microneedles. Int J Pharm 2009, 368(1-2):109-115.