Parasitic scabies mites and associated bacteria joining forces against host complement defence

Parasite Immunology

Volumn 36, Issue 11, 2014, Pages 585-593

  Swe, P M ^a   Reynolds, S L ^a   Fischer, K ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Coinfection disease; Complement immunological terms; Human host species; Sarcoptes parasite; Staphylococcus aureus bacteria; Streptococcus pyogenes bacteria

Indexed keywords

ACARI; BACTERIA (MICROORGANISMS); PSOROPTES CERVINUS; SARCOPTES; SARCOPTES SCABIEI; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PYOGENES;

COMPLEMENT;

ANIMAL; HUMAN; IMMUNE EVASION; IMMUNOLOGY; MIXED INFECTION; PARASITOLOGY; PHYSIOLOGY; SARCOPTES SCABIEI; SCABIES; SKIN INFECTION; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PYOGENES; VETERINARY;

ANIMALS; COINFECTION; COMPLEMENT SYSTEM PROTEINS; HUMANS; IMMUNE EVASION; SARCOPTES SCABIEI; SCABIES; SKIN DISEASES, INFECTIOUS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PYOGENES;

EID: 84922289209     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/pim.12133     Document Type: Article

References (99)

1. Samuel WM, Pybus MJ & Kocan AA. Parasitic Diseases of Wild Animals, 2nd edn. Ames, Iowa State University Press, 2001.
2. Currie B, Huffam S, O'Brien D & Walton S. Ivermectin for scabies. Lancet 1997; 350: 1551.
3. Worth C, Heukelbach J, Fengler G, Walter B, Liesenfeld O & Feldmeier H. Impaired quality of life in adults and children with scabies from an impoverished community in Brazil. Int J Dermatol 2012; 51: 275-282.
4. Engelman D, Kiang K, Chosidow O, et al. Toward the global control of human scabies: introducing the International Alliance for the Control of Scabies. PLoS Negl Trop Dis 2013; 7: e2167.
5. Fuller LC. Epidemiology of scabies. Curr Opin Infect Dis 2013; 26: 123-126.
6. Hay RJ, Steer AC, Engelman D & Walton S. Scabies in the developing world-its prevalence, complications, and management. Clin Microbiol Infect 2012; 18: 313-323.
7. Clucas DB, Carville KS, Connors C, Currie BJ, Carapetis JR & Andrews RM. Disease burden and health-care clinic attendances for young children in remote aboriginal communities of northern Australia. Bull World Health Organ 2008; 86: 275-281.
8. Carapetis JR, Connors C, Yarmirr D, Krause V & Currie BJ. Success of a scabies control program in an Australian aboriginal community. Pediatr Infect Dis J 1997; 16: 494-499.
9. Currie BJ & McCarthy JS. Permethrin and ivermectin for scabies. N Engl J Med 2010; 362: 717-725.
10. Carapetis JR, Steer AC, Mulholland EK & Weber M. The global burden of group A streptococcal diseases. Lancet Infect Dis 2005; 5: 685-694.
11. Lawrence G, Leafasia J, Sheridan J, et al. Control of scabies, skin sores and haematuria in children in the Solomon Islands: another role for ivermectin. Bull World Health Organ 2005; 83: 34-42.
12. Bergstrom FC, Reynolds S, Johnstone M, et al. Scabies mite inactivated serine protease paralogs inhibit the human complement system. J Immunol 2009; 182: 7809-7817.
13. Mika A, Reynolds SL, Mohlin FC, et al. Novel scabies mite serpins inhibit the three pathways of the human complement system. PLoS ONE 2012; 7: e40489.
14. Mika A, Reynolds SL, Pickering D, et al. Complement inhibitors from scabies mites promote streptococcal growth-a novel mechanism in infected epidermis? PLoS Negl Trop Dis 2012; 6: e1563.
15. Currie BJ & Carapetis JR. Skin infections and infestations in Aboriginal communities in northern Australia. Australas J Dermatol 2000; 41: 139-143; quiz 44-5.
16. Whitehall J, Kuzulugil D, Sheldrick K & Wood A. Burden of paediatric pyoderma and scabies in North West Queensland. J Paediatr Child Health 2013; 49: 141-143.
17. Rodriguez-Iturbe B & Musser JM. The current state of poststreptococcal glomerulonephritis. J Am Soc Nephrol 2008; 19: 1855-1864.
18. Hoy WE, White AV, Dowling A, et al. Post-streptococcal glomerulonephritis is a strong risk factor for chronic kidney disease in later life. Kidney Int 2012; 81: 1026-1032.
19. Tong SY, Bishop EJ, Lilliebridge RA, et al. Community-associated strains of methicillin-resistant Staphylococcus aureus and methicillin-susceptible S. aureus in indigenous Northern Australia: epidemiology and outcomes. J Infect Dis 2009; 199: 1461-1470.
20. Wong LC, Amega B, Connors C, et al. Outcome of an interventional program for scabies in an Indigenous community. Med J Aust 2001; 175: 367-370.
21. Scheinfeld N. Controlling scabies in institutional settings: a review of medications, treatment models, and implementation. Am J Clin Dermatol 2004; 5: 31-37.
22. Currie BJ, Harumal P, McKinnon M & Walton SF. First documentation of in vivo and in vitro ivermectin resistance in Sarcoptes scabiei. Clin Infect Dis 2004; 39: e8-e12.
23. Mounsey KE, Holt DC, McCarthy J, Currie BJ & Walton SF. Scabies: molecular perspectives and therapeutic implications in the face of emerging drug resistance. Future Microbiol 2008; 3: 57-66.
24. Mounsey KE, Holt DC, McCarthy JS, Currie BJ & Walton SF. Longitudinal evidence of increasing in vitro tolerance of scabies mites to ivermectin in scabies-endemic communities. Arch Dermatol 2009; 145: 840-841.
25. st century. Mol Immunol 2007; 44: 3838-3849.
26. Ehrnthaller C, Ignatius A, Gebhard F & Huber-Lang M. New insights of an old defense system: structure, function, and clinical relevance of the complement system. Mol Med 2011; 17: 317-329.
27. Makrides SC. Therapeutic inhibition of the complement system. Pharmacol Rev 1998; 50: 59-87.
28. Wallis R, Mitchell DA, Schmid R, Schwaeble WJ & Keeble AH. Paths reunited: Initiation of the classical and lectin pathways of complement activation. Immunobiology 2010; 215: 1-11.
29. Ricklin D, Hajishengallis G, Yang K & Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 2010; 11: 785-797.
30. Dahl MR, Thiel S, Matsushita M, et al. MASP-3 and its association with distinct complexes of the mannan-binding lectin complement activation pathway. Immunity 2001; 15: 127-135.
31. Sato T, Endo Y, Matsushita M & Fujita T. Molecular characterization of a novel serine protease involved in activation of the complement system by mannose-binding protein. Int Immunol 1994; 6: 665-669.
32. Thiel S, Vorup-Jensen T, Stover CM, et al. A second serine protease associated with mannan-binding lectin that activates complement. Nature 1997; 386: 506-510.
33. Chen CB & Wallis R. Two mechanisms for mannose-binding protein modulation of the activity of its associated serine proteases. J Biol Chem 2004; 279: 26058-26065.
34. Agarwal S, Ferreira VP, Cortes C, Pangburn MK, Rice PA & Ram S. An evaluation of the role of properdin in alternative pathway activation on Neisseria meningitidis and Neisseria gonorrhoeae. J Immunol 2010; 185: 507-516.
35. Cortes C, Ferreira VP & Pangburn MK. Native properdin binds to Chlamydia pneumoniae and promotes complement activation. Infect Immun 2011; 79: 724-731.
36. Fearon DT & Austen KF. Properdin: binding to C3b and stabilization of the C3b-dependent C3 convertase. J Exp Med 1975; 142: 856-863.
37. Ferreira VP, Cortes C & Pangburn MK. Native polymeric forms of properdin selectively bind to targets and promote activation of the alternative pathway of complement. Immunobiology 2010; 215: 932-940.
38. Gros P, Milder FJ & Janssen BJ. Complement driven by conformational changes. Nat Rev Immunol 2008; 8: 48-58.
39. Chesne S, Villiers CL, Arlaud GJ, Lacroix MB & Colomb MG. Fluid-phase interaction of C1 inhibitor (C1 Inh) and the subcomponents C1r and C1s of the first component of complement, C1. Biochem J 1982; 201: 61-70.
40. Skjoedt MO, Roversi P, Hummelshoj T, et al. Crystal structure and functional characterization of the complement regulator mannose-binding lectin (MBL)/ficolin-associated protein-1 (MAP-1). J Biol Chem 2012; 287: 32913-32921.
41. Ahearn JM & Rosengard AM. The Human Complement System in Health and Diseases. New York, Marcel Dekker, 1998: 167-202.
42. Wiesmann C, Katschke KJ, Yin J, et al. Structure of C3b in complex with CRIg gives insights into regulation of complement activation. Nature 2006; 444: 217-220.
43. Meri S, Morgan BP, Wing M, et al. Human protectin (CD59), an 18-20-kD homologous complement restriction factor, does not restrict perforin-mediated lysis. J Exp Med 1990; 172: 367-370.
44. Salo OP, Reunala T, Kalimo K & Rantanen T. Immunoglobulin and complement deposits in the skin and circulating immune complexes in scabies. Acta Derm Venereol 1982; 62: 73-76.
45. Hoefling KK & Schroeter AL. Dermatoimmunopathology of scabies. J Am Acad Dermatol 1980; 3: 237-240.
46. Frentz G, Veien NK & Eriksen K. Immunofluorescence studies in scabies. J Cutan Pathol 1977; 4: 191-193.
47. Arlian LG, Morgan MS, Vyszenski-Moher DL & Stemmer BL. Sarcoptes scabiei: the circulating antibody response and induced immunity to scabies. Exp Parasitol 1994; 78: 37-50.
48. Bos JD, Pasch MC & Asghar SS. Defensins and complement systems from the perspective of skin immunity and autoimmunity. Clin Dermatol 2001; 19: 563-572.
49. Rapp CM, Morgan MS & Arlian LG. Presence of host immunoglobulin in the gut of Sarcoptes scabiei (Acari: Sarcoptidae). J Med Entomol 2006; 43: 539-542.
50. Nunn MA, Sharma A, Paesen GC, et al. Complement inhibitor of C5 activation from the soft tick Ornithodoros moubata. J Immunol 2005; 174: 2084-2091.
51. Valenzuela JG, Charlab R, Mather TN & Ribeiro JM. Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. J Biol Chem 2000; 275: 18717-18723.
52. Tyson KR, Elkins C & de Silva AM. A novel mechanism of complement inhibition unmasked by a tick salivary protein that binds to properdin. J Immunol 2008; 180: 3964-3968.
53. Fischer K, Holt DC, Harumal P, Currie BJ, Walton SF & Kemp DJ. Generation and characterization of cDNA clones from Sarcoptes scabiei var. hominis for an expressed sequence tag library: identification of homologues of house dust mite allergens. Am J Trop Med Hyg 2003; 68: 61-64.
54. Holt D, Fischer K, Allen G, et al. Mechanisms for a novel immune evasion strategy in the scabies mite Sarcoptes scabiei: a multigene family of inactivated serine proteases. J Invest Dermatol 2003; 121: 1419-1424.
55. Reynolds SL, Pike RN, Mika A, et al. Scabies mite inactive serine proteases are potent inhibitors of the human complement lectin pathway. PLoS Negl Trop Dis 2014; 8: e2872.
56. Arlian LG, Estes SA & Vyszenski-Moher DL. Prevalence of Sarcoptes scabiei in the homes and nursing homes of scabietic patients. J Am Acad Dermatol 1988 (5 Pt 1); 19: 806-811.
57. Van Neste DLJ. Host-parasite relationships in hyperkeratotic (Norwegian) scabies: pathological and immunological findings. Br J Dermatol 1981; 105: 667-678.
58. Willis C, Fischer K, Walton SF, Currie BJ & Kemp DJ. Scabies mite inactivated serine protease paralogues are present both internally in the mite gut and externally in feces. Am J Trop Med Hyg 2006; 75: 683-687.
59. Mika A, Goh P, Holt DC, Kemp DJ & Fischer K. Scabies mite peritrophins are potential targets of human host innate immunity. PLoS Negl Trop Dis 2011; 5: e1331.
60. Swe PM, Zakrzewski M, Kelly A, Krause L & Fischer K. Scabies mites alter the skin microbiome and promote growth of opportunistic pathogens in a porcine model. PLoS Negl Trop Dis 2014; 8: e2897.
61. Van Neste DJ & Staquet MJ. Similar epidermal changes in hyperkeratotic scabies of humans and pigs. Am J Dermatopathol 1986; 8: 267-273.
62. Steinstraesser L, Vranckx JJ, Mohammadi-Tabrisi A, et al. A novel titanium wound chamber for the study of wound infections in pigs. Comp Med 2006; 56: 279-285.
63. Sullivan TP, Eaglstein WH, Davis SC & Mertz P. The pig as a model for human wound healing. Wound Repair Regen 2001; 9: 66-76.
64. Salvesen B & Mollnes TE. Pathway-specific complement activity in pigs evaluated with a human functional complement assay. Mol Immunol 2009; 46: 1620-1625.
65. Swe PM & Fischer K. A scabies mite serpin interferes with complement-mediated neutrophil functions and promotes staphylococcal growth. PLoS Negl Trop Dis 2014; 8: e2928.
66. Blom AM, Hallstrom T & Riesbeck K. Complement evasion strategies of pathogens-acquisition of inhibitors and beyond. Mol Immunol 2009; 46: 2808-2817.
67. Laarman A, Milder F, van Strijp J & Rooijakkers S. Complement inhibition by gram-positive pathogens: molecular mechanisms and therapeutic implications. J Mol Med 2010; 88: 115-120.
68. Serruto D, Rappuoli R, Scarselli M, Gros P & van Strijp JA. Molecular mechanisms of complement evasion: learning from staphylococci and meningococci. Nat Rev Microbiol 2010; 8: 393-399.
69. Lambris JD, Ricklin D & Geisbrecht BV. Complement evasion by human pathogens. Nat Rev Microbiol 2008; 6: 132-142.
70. Forsgren A & Sjoquist J. "Protein A" from S. aureus. I. Pseudo-immune reaction with human gamma-globulin. J Immunol 1966; 97: 822-827.
71. Goward CR, Scawen MD, Murphy JP & Atkinson T. Molecular evolution of bacterial cell-surface proteins. Trends Biochem Sci 1993; 18: 136-140.
72. Zhang L, Jacobsson K, Vasi J, Lindberg M & Frykberg L. A second IgG-binding protein in Staphylococcus aureus. Microbiology 1998; 144: 985-991.
73. Rooijakkers SH, van Wamel WJ, Ruyken M, van Kessel KP & van Strijp JA. Anti-opsonic properties of staphylokinase. Microbes Infect 2005; 7: 476-484.
74. von Pawel-Rammingen U & Bjorck L. IdeS and SpeB: immunoglobulin-degrading cysteine proteinases of Streptococcus pyogenes. Curr Opin Microbiol 2003; 6: 50-55.
75. Podbielski A, Schnitzler N, Beyhs P & Boyle MD. M-related protein (Mrp) contributes to group A streptococcal resistance to phagocytosis by human granulocytes. Mol Microbiol 1996; 19: 429-441.
76. Rooijakkers SH, Ruyken M, Roos A, et al. Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat Immunol 2005; 6: 920-927.
77. Jongerius I, Puister M, Wu J, Ruyken M, van Strijp JA & Rooijakkers SH. Staphylococcal complement inhibitor modulates phagocyte responses by dimerization of convertases. J Immunol 2010; 184: 420-425.
78. Rooijakkers SH, van Kessel KP & van Strijp JA. Staphylococcal innate immune evasion. Trends Microbiol 2005; 13: 596-601.
79. Jongerius I, Kohl J, Pandey MK, et al. Staphylococcal complement evasion by various convertase-blocking molecules. J Exp Med 2007; 204: 2461-2471.
80. Jongerius I, Garcia BL, Geisbrecht BV, van Strijp JA & Rooijakkers SH. Convertase inhibitory properties of Staphylococcal extracellular complement-binding protein. J Biol Chem 2010; 285: 14973-14979.
81. Bestebroer J, Aerts PC, Rooijakkers SH, et al. Functional basis for complement evasion by staphylococcal superantigen-like 7. Cell Microbiol 2010; 12: 1506-1516.
82. Chmouryguina I, Suvorov A, Ferrieri P & Cleary PP. Conservation of the C5a peptidase genes in group A and B streptococci. Infect Immun 1996; 64: 2387-2390.
83. Berends ET, Dekkers JF, Nijland R, et al. Distinct localization of the complement C5b-9 complex on Gram-positive bacteria. Cell Microbiol 2013; 15: 1955-1968.
84. Fernie-King BA, Seilly DJ, Willers C, Wurzner R, Davies A & Lachmann PJ. Streptococcal inhibitor of complement (SIC) inhibits the membrane attack complex by preventing uptake of C567 onto cell membranes. Immunology 2001; 103: 390-398.
85. Laursen NS, Gordon N, Hermans S, et al. Structural basis for inhibition of complement C5 by the SSL7 protein from Staphylococcus aureus. Proc Natl Acad Sci U S A 2010; 107: 3681-3686.
86. Sharp JA, Echague CG, Hair PS, et al. Staphylococcus aureus surface protein SdrE binds complement regulator factor H as an immune evasion tactic. PLoS ONE 2012; 7: e38407.
87. Haupt K, Reuter M, van den Elsen J, et al. The Staphylococcus aureus protein Sbi acts as a complement inhibitor and forms a tripartite complex with host complement Factor H and C3b. PLoS Pathog 2008; 4: e1000250.
88. Laarman AJ, Ruyken M, Malone CL, van Strijp JA, Horswill AR & Rooijakkers SH. Staphylococcus aureus metalloprotease aureolysin cleaves complement C3 to mediate immune evasion. J Immunol 2011; 186: 6445-6453.
89. Hair PS, Echague CG, Sholl AM, et al. Clumping factor A interaction with complement factor I increases C3b cleavage on the bacterial surface of Staphylococcus aureus and decreases complement-mediated phagocytosis. Infect Immun 2010; 78: 1717-1727.
90. Thern A, Stenberg L, Dahlback B & Lindahl G. Ig-binding surface proteins of Streptococcus pyogenes also bind human C4b-binding protein (C4BP), a regulatory component of the complement system. J Immunol 1995; 154: 375-386.
91. Tsao N, Tsai WH, Lin YS, Chuang WJ, Wang CH & Kuo CF. Streptococcal pyrogenic exotoxin B cleaves properdin and inhibits complement-mediated opsonophagocytosis. Biochem Biophys Res Commun 2006; 339: 779-784.
92. Gordon DL, Rice JL & McDonald PJ. Regulation of human neutrophil type 3 complement receptor (iC3b receptor) expression during phagocytosis of Staphylococcus aureus and Escherichia coli. Immunology 1989; 67: 460-465.
93. Fossati-Jimack L, Ling GS, Cortini A, et al. Phagocytosis is the main CR3-mediated function affected by the lupus-associated variant of CD11b in human myeloid cells. PLoS ONE 2013; 8: e57082.
94. Gerard C & Gerard NP. C5A anaphylatoxin and its seven transmembrane-segment receptor. Annu Rev Immunol 1994; 12: 775-808.
95. Postma B, Kleibeuker W, Poppelier MJ, et al. Residues 10-18 within the C5a receptor N terminus compose a binding domain for chemotaxis inhibitory protein of Staphylococcus aureus. J Biol Chem 2005; 280: 2020-2027.
96. Lei B, DeLeo FR, Hoe NP, et al. Evasion of human innate and acquired immunity by a bacterial homolog of CD11b that inhibits opsonophagocytosis. Nat Med 2001; 7: 1298-1305.
97. Podbielski A, Peterson JA & Cleary P. Surface protein-CAT reporter fusions demonstrate differential gene expression in the vir regulon of Streptococcus pyogenes. Mol Microbiol 1992; 6: 2253-2265.
98. Pritchard KH & Cleary PP. Differential expression of genes in the vir regulon of Streptococcus pyogenes is controlled by transcription termination. Mol Gen Genet 1996; 250: 207-213.
99. Rooijakkers SH, Ruyken M, van Roon J, van Kessel KP, van Strijp JA & van Wamel WJ. Early expression of SCIN and CHIPS drives instant immune evasion by Staphylococcus aureus. Cell Microbiol 2006; 8: 1282-1293.