#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Distinct Upstream Role of Type I IFN Signaling in Hematopoietic Stem Cell-Derived and Epithelial Resident Cells for Concerted Recruitment of Ly-6C Monocytes and NK Cells via CCL2-CCL3 Cascade


Herpes simplex virus type 1 and 2 (HSV-1 and HSV-2) are the most common cause of genital ulceration in humans worldwide with lifelong latent infection after peripheral replication in mucosal tissues. Furthermore, acquisition of human immunodeficiency virus (HIV) is increased in HSV-infected individuals, underscoring the contribution of this virus in facilitating increased susceptibility to other microbial pathogens. Therefore, it is imperative to characterize the host defense to HSV infection and identify key components that regulate virus resistance, in order to devise therapeutic strategy. Although type I interferon (IFN-I)-dependent orchestrated mobilization of innate cells in inflamed tissues is considered a key player to control replication and CNS-invasion of HSV, the regulators and cell population that are affected by IFN-I to establish the orchestrated environment of innate cells in HSV-infected tissues are largely unknown. In the present study, we demonstrate that IFN-I signal governs the sequential recruitment of Ly-6Chi monocytes and then NK cells into mucosal tissues, depending on CCL2-CCL3 cascade mediated by HSC-derived leukocytes and epithelial resident cells, respectively. Also, tissue resident CD11bhiF4/80hi macrophages and CD11chiEpCAM+ dendritic cells were involved in producing the initial CCL2 for migration-based self-amplification of rapidly infiltrated Ly-6Chi monocytes through stimulation by IFN-I produced from infected epithelial cells. This study deciphers detailed IFN-I-dependent pathway that establishes orchestrated mobilization of Ly-6Chi monocytes and NK cells through CCL2-CCL3 cascade.


Vyšlo v časopise: Distinct Upstream Role of Type I IFN Signaling in Hematopoietic Stem Cell-Derived and Epithelial Resident Cells for Concerted Recruitment of Ly-6C Monocytes and NK Cells via CCL2-CCL3 Cascade. PLoS Pathog 11(11): e32767. doi:10.1371/journal.ppat.1005256
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005256

Souhrn

Herpes simplex virus type 1 and 2 (HSV-1 and HSV-2) are the most common cause of genital ulceration in humans worldwide with lifelong latent infection after peripheral replication in mucosal tissues. Furthermore, acquisition of human immunodeficiency virus (HIV) is increased in HSV-infected individuals, underscoring the contribution of this virus in facilitating increased susceptibility to other microbial pathogens. Therefore, it is imperative to characterize the host defense to HSV infection and identify key components that regulate virus resistance, in order to devise therapeutic strategy. Although type I interferon (IFN-I)-dependent orchestrated mobilization of innate cells in inflamed tissues is considered a key player to control replication and CNS-invasion of HSV, the regulators and cell population that are affected by IFN-I to establish the orchestrated environment of innate cells in HSV-infected tissues are largely unknown. In the present study, we demonstrate that IFN-I signal governs the sequential recruitment of Ly-6Chi monocytes and then NK cells into mucosal tissues, depending on CCL2-CCL3 cascade mediated by HSC-derived leukocytes and epithelial resident cells, respectively. Also, tissue resident CD11bhiF4/80hi macrophages and CD11chiEpCAM+ dendritic cells were involved in producing the initial CCL2 for migration-based self-amplification of rapidly infiltrated Ly-6Chi monocytes through stimulation by IFN-I produced from infected epithelial cells. This study deciphers detailed IFN-I-dependent pathway that establishes orchestrated mobilization of Ly-6Chi monocytes and NK cells through CCL2-CCL3 cascade.


Zdroje

1. Lee AJ, Ashkar AA. Herpes simplex virus-2 in the genital mucosa: insights into the mucosal host response and vaccine development. Curr. Opin. Infect. Dis. 2012; 25:92–99. doi: 10.1097/QCO.0b013e32834e9a56 22143115

2. Chentoufi AA, Benmohamed L. Mucosal herpes immunity and immunopathology to ocular and genital herpes simplex virus infections. Clin. Dev. Immunol. 2012;2012:149135. doi: 10.1155/2012/149135 23320014

3. Grinde B. Herpes viruses: latency and reactivation—viral strategies and host responses. J. Oral Microbiol. 2013; 25:5. doi: 10.3402/jom.v5i0.22766 24167660

4. Auvert B, Ballard R, Campbell C, Carael M, Carton M, Fehler G, et al. HIV infection among youth in a South African mining town is associated with herpes simplex virus-2 seropositivity and sexual behavior. AIDS 2001; 15:885–889. 11399961

5. Mugo N, Dadabhai SS, Bunnell R, Williamson J, Bennett E, Baya I, et al. Prevalence of herpes simplex virus type 2 infection, human immunodeficiency virus/herpes simplex virus type 2 coinfection, and associated risk factors in a national, population-based survey in Kenya. Sex Transm. Dis. 2011; 38:1059–1066. doi: 10.1097/OLQ.0b013e31822e60b6 21992985

6. Freeman EE, Weiss HA, Glynn JR, Cross PL, Whitworth JA, Hayes RJ. Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS 2006; 20: 73–83. 16327322.

7. Baker DA, Plotkin SA. Enhancement of vaginal infection in mice by herpes simplex virus type II with progesterone. Proc. Soc. Exp. Biol. Med. 1978; 158:131–134. 209470

8. Parr MB, Kepple L, McDermott MR, Drew MD, Bozzola JJ, Parr EL. A mouse model for studies of mucosal immunity to vaginal infection by herpes simplex virus type 2. Lab. Investig. 1994; 70:369–380. 8145530

9. Gill N, Rosenthal RL, Ashkar AA. NK and NKT cell independent contribution of interleukin-15 to innate protection against mucosal viral infection. J. Virol. 2005; 79:4470–4478. 15767447

10. Harandi AM, Svennerholm B, Holmgren J, Eriksson K. Interleukin-12 (IL-12) and IL-18 are important in innate defense against genital herpes simplex virus type 2 infection in mice but are not required for the development of acquired gamma interferon-mediated protective immunity. J. Virol. 2001; 75:6705–6709. 11413339

11. Milligan GN. Neutrophils aid in protection of the vaginal mucosae of immune mice against challenge with herpes simplex virus type 2. J. Virol. 1999; 73:6380–6386. 10400730

12. Conrady CD, Jones H, Zheng M, Carr DJJ. A functional type I interferon pathway drives resistance to cornea herpes simplex type 1 infection by recruitment of leukocytes. J. Biomed. Res. 2011; 25:111–119. 21709805

13. Conrady CD, Zheng M, Mandal NA, van Rooijen N, Carr DJJ. IFN-α-driven CCL2 production recruits inflammatory monocytes to infection site in mice. Mucosal Immunol. 2013; 6:45–55. doi: 10.1038/mi.2012.46 22692455

14. Harandi AM, Svennerholm B, Holmgren J, Eriksson K. Differential roles B cells and IFN-γ secreting CD4+T cells in innate and adaptive immune control of genital herpes simplex virus type 2 infection in mice. J. Gen. Virol. 2001; 82:845–853. 11257190

15. Milligan GN, Bernstein DI. Interferon- γ enhances resolution of herpes simplex virus type 2 infection of the murine genital tract. Virology 1997; 229:259–268. 9123869

16. Parr MB, Parr EL. The role of gamma interferon in immune resistance to vaginal infection by herpes simplex virus type 2 in mice. Virology 1999; 258:282–294. 10366565

17. Nandakumar S, Woolard SN, Yuan D, Rouse BT, Kumaraguru U. Natural killer cells as novel helpers in anti-herpes simplex virus immune response. J. Virol. 2008; 82:10820–10831. doi: 10.1128/JVI.00365-08 18715907

18. Gill N, Chenoweth MJ, Verdu EF, and Ashkar AA. NK cells require type I IFN receptor for antiviral responses during genital HSV-2 infection. Cell. Immunol. 2011; 269:29–37. doi: 10.1016/j.cellimm.2011.03.007 21477795

19. Kim M, Osborne NR, Zeng W, Donaghy H, McKinnon K, Jackson DC, et al. Herpes simplex virus antigens directly activate NK cells via TLR2, thus facilitating their presentation to CD4 T lymphocytes. J. Immunol. 2012; 188:4158–70. doi: 10.4049/jimmunol.1103450 22467654

20. Beuneu H, Deguine J, Bouvier I, Di Santo JP, Albert ML, Bousso P. Cutting Edge: A dual role for Type I IFNs during Polyinosinic-polycytidylic acid-induced NK cell activation. J. Immunol. 2011; 187:2084–2088. doi: 10.4049/jimmunol.1004210 21810605

21. Baranek T, Vu Manh T-P, Alexandre Y, Maqbool MA, Cabeza JZ, Tomasello E, et al. Differential responses of immune cells to type I interferon contribute to host resistance to viral infection. Cell Host & Microbe 2012; 12: 571–584. doi: 10.1016/j.chom.2012.09.002 23084923

22. Osterholzer JJ, Chen GH, Olszewski MA, Zhang YM, Curtis JL, Huffnagle GB, et al. Chemokine receptor 2- mediated accumulation of fungicidal exudate macrophage in mice that clear cryptococcal lung infection. Am. J. Pathol. 2011; 178: 198–211. doi: 10.1016/j.ajpath.2010.11.006 21224057

23. D’Agostino PM, Kwak C, Vecchiarelli HA, Toth JG, Miller JM, Masheeb Z, et al. Viral-induced encephalitis initiates distinct and functional CD103+CD11b+ brain dendritic cell populations within the olfactory bulb. Proc. Natl. Acad. Sci. USA. 2012; 109:175–180. doi: 10.1073/pnas.1203941109 22474352

24. Serbina NV, Pamer EG. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 2006; 7:311–317. 16462739

25. Serbina NV, Salazar-Mather TP, Biron CA, Kuziel WA, Pamer EG. TNF/iNOS producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 2003; 19:59–70. 12871639

26. Dunay IR, Damatta RA, Fux B, Presti R, Grecos S, Conna M, et al. Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 2008; 29:306–317. doi: 10.1016/j.immuni.2008.05.019 18691912

27. León B, López-Bravo M, Ardavín C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 2007; 26:519–531. 17412618

28. Iijima N, Lisa MM, Iwasaki A. Recruited inflammatory monocytes stimulate antiviral Th1 immunity in infected tissue. Proc Natl Acad Sci USA. 2011; 108: 284–289. doi: 10.1073/pnas.1005201108 21173243

29. Seo SU, Kwon HJ, Ko HJ, Byun YH, Seong BL, Uematsu S, et al. Type I interferon signaling regulates Ly6Chi Monocytes and Neutrophils during acute viral Pneumonia in mice. PLoS Pathog. 2011; 7: e1001304. doi: 10.1371/journal.ppat.1001304 21383977

30. Crane MJ, Hokeness-Antonelli KL, Salazar-Mather TP. Regulation of inflammatory monocyte/macrophage recruitment from the bone marrow during murine cytomegalovirus infection: role for type I interferons in localized induction of CCR2 ligands. J. Immunol. 2009; 183:2810–2817. doi: 10.4049/jimmunol.0900205 19620305

31. Lee PY, Li Y, Kumagai Y, Xu Y, Weinstein JS, Kellner ES, et al. Type I IFN modulates monocyte recruitment and maturation in chronic inflammation. Am. J. Pathol. 2009; 175:2023–2033. doi: 10.2353/ajpath.2009.090328 19808647

32. Meloni F, Solari N, Miserere S, Morosini M, Cascina A, Klersy C, et al. Chemokine redundancy in BOS pathogenesis. A possible role also for the CC chemokines: MIP3-beta, MIP9-alpha, MDC and their specific receptors. Transpl. Immunol. 2008; 18: 275–280. 18047937

33. Colobran R, Pujol-Borrell R, Armengol MP, Juan M. The chemokine network. I. How the genomic organization of chemokines contains clues for deciphering their functional complexity. Clin. Exp. Immunol. 2007; 148:208–17. 17437419

34. Orzalli MH, DeLuca NA, Knipe DM. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc. Natl. Acad. Sci. USA. 2012; 109:E3008–3017. doi: 10.1073/pnas.1211302109 23027953

35. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461:788–792. doi: 10.1038/nature08476 19776740

36. Du C, Wang P, Yu Y, Chen F, Liu J, Li Y. Gadolinium chloride improves the course of TNBS and DSS-induced colitis through protecting against colonic mucosal inflammation. Sci. Rep. 2014; 4:6096. doi: 10.1038/srep06096 25146101

37. Amoura Z, Combadiere C, Faure S, Parizot C, Miyara M, Raphaël D, et al. Roles of CCR2 and CXCR3 in the T cell-mediated response occurring during lupus flares. Arthritis Rheum. 2003; 48:3487–3496. 14673999

38. Flaishon L, Becker-Herman S, Hart G, Levo Y, Kuziel WA, Shachar I. Expression of the chemokine receptor CCR2 on immature B cells negatively regulates their cytoskeletal rearrangement and migration. Blood 2004; 104: 933–941. 15126315

39. Thomas SY, Hou R, Boyson JE, Means TK, Hess C, Olson DP, et al. CD1d-restricted NKT cells express a chemokine receptor profile indicative of Th1-type inflammatory homing cells. J. Immunol. 2003; 171:2571–2580. 12928408

40. Thapa M, Kuziel WA, Carr DJJ. Susceptibility of CCR5-deficient mice to genital herpes simplex virus type 2 is linked to NK cell mobilization. J. Virol. 2007; 81:3704–3713. 17267483

41. Salazar-Mather TP, Lewis CA, Biron CA. Type I interferons regulate inflammatory cell trafficking and macrophage inflammatory protein 1α delivery to the liver. J. Clin. Invest. 2002; 110:321–330. 12163451

42. Salazar-Mather TP, Hamilton T, Biron CA. A chemokine-to-cytokine-to-chemokine cascade critical in antiviral defense. J. Clin. Invest. 2000; 105:985–993. 10749577

43. Thapa M, Welner RS, Pelayo R, Carr DJJ. CXCL9 and CXCL10 expression are critical for control of genital herpes simplex virus type 2 infection through mobilization of HSV-specific CTL and NK cells to the nervous system. J. Immunol. 2008; 180:1098–1106. 18178850

44. Dorhoi A, Yeremeev V, Nouailles G, Weiner J 3rd, Jorg S, Heinemann E, et al. Type I IFN signaling triggers immunopathology in tuberculosis-susceptible mice by modulating lung phagocyte dynamics. Eur. J. Immunol. 2014; 44:2380–2390.24782112

45. Yang Q, Ghose P, Ismail N. Neutrophils mediate immunopathology and negative regulate protective immune responses during fatal bacterial infection-induced toxic shock. Infect. Immun. 2013; 81:1751–1763. doi: 10.1128/IAI.01409-12 23478316

46. Weighardt H, Kaiser-Moore S, Schlautkotter S, Rossmann-Bloeck T, Schleicher U, Bogdan C, et al. Type I IFN modulates host defense and late hyper inflammation in septic peritonitis. J. Immunol. 2006; 177:5623–5630. 17015750

47. Kelly-Scumpia KM, Scumpia PO, Delano MJ, Weinstein JS, Cuenca AG, Wynn JL, et al. Type I interferon signaling in hematopoietic cells is required for survival in mouse polymicrobial sepsis by regulating CXCL10. J. Exp. Med. 2010; 207:319–326. doi: 10.1084/jem.20091959 20071504

48. Stock AT, Smith JM, Carbone FR. Type I IFN suppresses CXCR2 driven neutrophil recruitment into the sensory ganglia during viral infection. J. Exp. Med. 2014; 211:751–759. doi: 10.1084/jem.20132183 24752295

49. Majer O, Bourgeois C, Zwolanek F, Lassing C, Kerjaschki D, Mack M, et al. Type I interferons promote fatal immunopathology by regulating inflammatory monocytes and neutrophils during candida infections. PLoS Pathog. 2012; 8:e1002811. doi: 10.1371/journal.ppat.1002811 22911155

50. Conrady CD, Zheng M, Fitzgerald KA, Liu C, Carr DJJ. Resistance to HSV-1 infection in the epithelium resides with the novel innate sensor, IFI-16. Mucosal Immunol. 2012; 5: 173–183. doi: 10.1038/mi.2011.63 22236996

51. Hokeness KL, Kuziel WA, Biron CA, Salazar-Mather TP. Monocyte chemoattractant protein-1 and CCR2 interactions are required for IFN-α/β- induced inflammatory responses and antiviral defense in liver. J. Immunol. 2005; 174:1549–1556. 15661915

52. Khorooshi R, Babcock AA, Owens T. NF-kappaB-driven STAT2 and CCL2 expression in astrocytes in response to brain injury. J. Immunol. 2008; 181: 7284–7291. 18981150

53. Bonello GB, Pham MH, Begum K, Sigala J, Sataranatarajan K, Mummidi S. An evolutionarily conserved TNF-alpha-responsive enhancer in the far upstream region of human CCL2 locus infl uences its gene expression. J. Immunol. 2011; 186: 7025–7038. doi: 10.4049/jimmunol.0900643 21551367

54. Zhao X, Deak E, Soderberg K, Linehan M, Spezzano D, Zhu J, et al. Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J. Exp. Med. 2003; 197:153–162. 12538655

55. Tumpey TM, Chen SH, Oakes JE, Lausch RN. Neutrophil mediated suppression of virus replication after herpes simplex virus type 1 infection of the murine cornea. J. Virol. 1996; 70: 898–904. 8551629

56. Siebens H, Tevethia SS, Babior BM. Neutrophil-mediated antibody dependent killing of herpes-simplex-virus-infected cells. Blood 1974; 54: 88–94. 221057

57. Gaaajetaaan GR, Geelen TH, Grauls GE, Bruggeman CA, Stassen FR. CpG and poly (I:C) stimulation of dendritic cells and fibroblasts limits herpes simplex virus type 1 infection in an IFNβ-dependent and –independent way. Antiviral Res. 2012; 93:39–47. doi: 10.1016/j.antiviral.2011.10.015 22057305

58. Low-Calle AM, Prada-Arismendy J, Castellanos JE. Study of interferon-β antiviral activity against Herpes simplex virus type 1 in neuron-enriched trigeminal ganglia cultures. Virus Res. 2014; 180:49–58. doi: 10.1016/j.virusres.2013.12.022 24374267

59. Giron-Michel J, Weill D, Bailly G, Legras S, Nardeux PC, Azzarone B et al. Direct signal transduction via functional interferon-αβ receptors in CD34+ hematopoietic stem cells. Leukemia 2002; 16:1135–1142. 12040445

60. Esser MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, et al. IFNalpha activates dormant hematopoietic stem cell in vivo. Nature 2009; 458:904–908. doi: 10.1038/nature07815 19212321

61. Sato T, Onai N, Yoshihara H, Arai F, Suda T, Ohteki T. Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat. Med. 2009; 15:696–700. doi: 10.1038/nm.1973 19483695

62. Aleyas AG, Han YW, George JA, Kim B, Kim K, Lee CK, et al. Multifront assault on antigen presentation by Japanese encephalitis virus subverts CD8+T cell responses. J. Immunol. 2010; 185:1429–41. doi: 10.4049/jimmunol.0902536 20581148

63. Eo SK, Lee S, Chun S, Rouse BT. Modulation of immunity against herpes simplex virus infection via mucosal genetic transfer of plasmid DNA encoding chemokines. J. Virol. 2001; 75:569–78. 11134269

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2015 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#