A Novel Pseudopodial Component of the Dendritic Cell Anti-Fungal Response: The Fungipod
Fungal pathologies are seen in immunocompromised and healthy humans. C-type lectins expressed on immature dendritic cells (DC) recognize fungi. We report a novel dorsal pseudopodial protrusion, the “fungipod”, formed by DC after contact with yeast cell walls. These structures have a convoluted cell-proximal end and a smooth distal end. They persist for hours, exhibit noticeable growth and total 13.7±5.6 µm long and 1.8±0.67 µm wide at the contact. Fungipods contain clathrin and an actin core surrounded by a sheath of cortactin. The actin cytoskeleton, but not microtubules, is required for fungipod integrity and growth. An apparent rearward flow (225±55 nm/second) exists from the zymosan contact site into the distal fungipod. The phagocytic receptor Dectin-1 is not required for fungipod formation, but CD206 (Mannose Receptor) is the generative receptor for these protrusions. The human pathogen Candida parapsilosis induces DC fungipod formation strongly, but the response is species specific since the related fungal pathogens Candida tropicalis and Candida albicans induce very few and no fungipods, respectively. Our findings show that fungipods are dynamic actin-driven cellular structures involved in fungal recognition by DC. They may promote yeast particle phagocytosis by DC and are a specific response to large (i.e., 5 µm) particulate ligands. Our work also highlights the importance of this novel protrusive structure to innate immune recognition of medically significant Candida yeasts in a species specific fashion.
Vyšlo v časopise:
A Novel Pseudopodial Component of the Dendritic Cell Anti-Fungal Response: The Fungipod. PLoS Pathog 6(2): e32767. doi:10.1371/journal.ppat.1000760
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000760
Souhrn
Fungal pathologies are seen in immunocompromised and healthy humans. C-type lectins expressed on immature dendritic cells (DC) recognize fungi. We report a novel dorsal pseudopodial protrusion, the “fungipod”, formed by DC after contact with yeast cell walls. These structures have a convoluted cell-proximal end and a smooth distal end. They persist for hours, exhibit noticeable growth and total 13.7±5.6 µm long and 1.8±0.67 µm wide at the contact. Fungipods contain clathrin and an actin core surrounded by a sheath of cortactin. The actin cytoskeleton, but not microtubules, is required for fungipod integrity and growth. An apparent rearward flow (225±55 nm/second) exists from the zymosan contact site into the distal fungipod. The phagocytic receptor Dectin-1 is not required for fungipod formation, but CD206 (Mannose Receptor) is the generative receptor for these protrusions. The human pathogen Candida parapsilosis induces DC fungipod formation strongly, but the response is species specific since the related fungal pathogens Candida tropicalis and Candida albicans induce very few and no fungipods, respectively. Our findings show that fungipods are dynamic actin-driven cellular structures involved in fungal recognition by DC. They may promote yeast particle phagocytosis by DC and are a specific response to large (i.e., 5 µm) particulate ligands. Our work also highlights the importance of this novel protrusive structure to innate immune recognition of medically significant Candida yeasts in a species specific fashion.
Zdroje
1. BanerjeeSN
EmoriTG
CulverDH
GaynesRP
JarvisWR
1991 Secular trends in nosocomial primary bloodstream infections in the United States, 1980–1989. National Nosocomial Infections Surveillance System. Am J Med 91 86S 89S
2. Beck-SagueC
JarvisWR
1993 Secular trends in the epidemiology of nosocomial fungal infections in the United States, 1980–1990. National Nosocomial Infections Surveillance System. J Infect Dis 167 1247 1251
3. TrofaD
GacserA
NosanchukJD
2008 Candida parapsilosis, an emerging fungal pathogen. Clin Microbiol Rev 21 606 625
4. LesageG
BusseyH
2006 Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70 317 343
5. NguyenTH
FleetGH
RogersPL
1998 Composition of the cell walls of several yeast species. Appl Microbiol Biotechnol 50 206 212
6. WillmentJA
BrownGD
2008 C-type lectin receptors in antifungal immunity. Trends Microbiol 16 27 32
7. CambiA
de LangeF
van MaarseveenNM
NijhuisM
JoostenB
2004 Microdomains of the C-type lectin DC-SIGN are portals for virus entry into dendritic cells. J Cell Biol 164 145 155
8. CambiA
NeteaMG
Mora-MontesHM
GowNA
HatoSV
2008 Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J Biol Chem 283 20590 20599
9. TaylorPR
GordonS
Martinez-PomaresL
2005 The mannose receptor: linking homeostasis and immunity through sugar recognition. Trends Immunol 26 104 110
10. StahlPD
EzekowitzRA
1998 The mannose receptor is a pattern recognition receptor involved in host defense. Curr Opin Immunol 10 50 55
11. ShibataY
MetzgerWJ
MyrvikQN
1997 Chitin particle-induced cell-mediated immunity is inhibited by soluble mannan: mannose receptor-mediated phagocytosis initiates IL-12 production. J Immunol 159 2462 2467
12. YamamotoY
KleinTW
FriedmanH
1997 Involvement of mannose receptor in cytokine interleukin-1beta (IL-1beta), IL-6, and granulocyte-macrophage colony-stimulating factor responses, but not in chemokine macrophage inflammatory protein 1beta (MIP-1beta), MIP-2, and KC responses, caused by attachment of Candida albicans to macrophages. Infect Immun 65 1077 1082
13. GarnerRE
RubanowiceK
SawyerRT
HudsonJA
1994 Secretion of TNF-alpha by alveolar macrophages in response to Candida albicans mannan. J Leukoc Biol 55 161 168
14. GiaimisJ
LombardY
FonteneauP
MullerCD
LevyR
1993 Both mannose and beta-glucan receptors are involved in phagocytosis of unopsonized, heat-killed Saccharomyces cerevisiae by murine macrophages. J Leukoc Biol 54 564 571
15. LanzavecchiaA
1996 Mechanisms of antigen uptake for presentation. Curr Opin Immunol 8 348 354
16. ShepherdVL
HoidalJR
1990 Clearance of neutrophil-derived myeloperoxidase by the macrophage mannose receptor. Am J Respir Cell Mol Biol 2 335 340
17. RijkenDC
OtterM
KuiperJ
van BerkelTJ
1990 Receptor-mediated endocytosis of tissue-type plasminogen activator (t-PA) by liver cells. Thromb Res Suppl 10 63 71
18. EastL
IsackeCM
2002 The mannose receptor family. Biochim Biophys Acta 1572 364 386
19. WeaverAM
KarginovAV
KinleyAW
WeedSA
LiY
2001 Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 11 370 374
20. UrunoT
LiuJ
ZhangP
FanY
EgileC
2001 Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat Cell Biol 3 259 266
21. SelbachM
BackertS
2005 Cortactin: an Achilles' heel of the actin cytoskeleton targeted by pathogens. Trends Microbiol 13 181 189
22. WeedSA
KarginovAV
SchaferDA
WeaverAM
KinleyAW
2000 Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J Cell Biol 151 29 40
23. CantarelliVV
TakahashiA
AkedaY
NagayamaK
HondaT
2000 Interaction of enteropathogenic or enterohemorrhagic Escherichia coli with HeLa cells results in translocation of cortactin to the bacterial adherence site. Infect Immun 68 382 386
24. FrischknechtF
WayM
2001 Surfing pathogens and the lessons learned for actin polymerization. Trends Cell Biol 11 30 38
25. DalyRJ
2004 Cortactin signalling and dynamic actin networks. Biochem J 382 13 25
26. CampbellDH
SutherlandRL
DalyRJ
1999 Signaling pathways and structural domains required for phosphorylation of EMS1/cortactin. Cancer Res 59 5376 5385
27. WeedSA
DuY
ParsonsJT
1998 Translocation of cortactin to the cell periphery is mediated by the small GTPase Rac1. J Cell Sci 111 (Pt 16) 2433 2443
28. WuH
ParsonsJT
1993 Cortactin, an 80/85-kilodalton pp60src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J Cell Biol 120 1417 1426
29. Cosen-BinkerLI
KapusA
2006 Cortactin: the gray eminence of the cytoskeleton. Physiology (Bethesda) 21 352 361
30. ChenL
WangZW
ZhuJW
ZhanX
2006 Roles of cortactin, an actin polymerization mediator, in cell endocytosis. Acta Biochim Biophys Sin (Shanghai) 38 95 103
31. McNivenMA
KimL
KruegerEW
OrthJD
CaoH
2000 Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151 187 198
32. GantnerBN
SimmonsRM
UnderhillDM
2005 Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J 24 1277 1286
33. BrownGD
GordonS
2001 Immune recognition. A new receptor for beta-glucans. Nature 413 36 37
34. SungSS
NelsonRS
SilversteinSC
1983 Yeast mannans inhibit binding and phagocytosis of zymosan by mouse peritoneal macrophages. J Cell Biol 96 160 166
35. HorwitzMA
1984 Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell 36 27 33
36. d'OstianiCF
Del SeroG
BacciA
MontagnoliC
SprecaA
2000 Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans. Implications for initiation of T helper cell immunity in vitro and in vivo. J Exp Med 191 1661 1674
37. RittigMG
SchroppelK
SeackKH
SanderU
N'DiayeEN
1998 Coiling phagocytosis of trypanosomatids and fungal cells. Infect Immun 66 4331 4339
38. RittigMG
BurmesterGR
KrauseA
1998 Coiling phagocytosis: when the zipper jams, the cup is deformed. Trends Microbiol 6 384 388
39. LoHJ
KohlerJR
DiDomenicoB
LoebenbergD
CacciapuotiA
1997 Nonfilamentous C. albicans mutants are avirulent. Cell 90 939 949
40. CowiesonNP
KingG
CooksonD
RossI
HuberT
2008 Cortactin adopts a globular conformation and bundles actin into sheets. J Biol Chem 283 16187 16193
41. HuangC
LiuJ
HaudenschildCC
ZhanX
1998 The role of tyrosine phosphorylation of cortactin in the locomotion of endothelial cells. J Biol Chem 273 25770 25776
42. HeinsbroekSE
TaylorPR
MartinezFO
Martinez-PomaresL
BrownGD
2008 Stage-specific sampling by pattern recognition receptors during Candida albicans phagocytosis. PLoS Pathog 4 e1000218 doi:10.1371/journal.ppat.1000218
43. MerrifieldCJ
MossSE
BallestremC
ImhofBA
GieseG
1999 Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat Cell Biol 1 72 74
44. CudmoreS
CossartP
GriffithsG
WayM
1995 Actin-based motility of vaccinia virus. Nature 378 636 638
45. TheriotJA
1995 The cell biology of infection by intracellular bacterial pathogens. Annu Rev Cell Dev Biol 11 213 239
46. ShenoyVB
TambeDT
PrasadA
TheriotJA
2007 A kinematic description of the trajectories of Listeria monocytogenes propelled by actin comet tails. Proc Natl Acad Sci U S A 104 8229 8234
47. GouinE
GanteletH
EgileC
LasaI
OhayonH
1999 A comparative study of the actin-based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii. J Cell Sci 112 (Pt 11) 1697 1708
48. Bernheim-GroswasserA
WiesnerS
GolsteynRM
CarlierMF
SykesC
2002 The dynamics of actin-based motility depend on surface parameters. Nature 417 308 311
49. FrischknechtF
CudmoreS
MoreauV
ReckmannI
RottgerS
1999 Tyrosine phosphorylation is required for actin-based motility of vaccinia but not Listeria or Shigella. Curr Biol 9 89 92
50. CameronLA
SvitkinaTM
VignjevicD
TheriotJA
BorisyGG
2001 Dendritic organization of actin comet tails. Curr Biol 11 130 135
51. TauntonJ
RowningBA
CoughlinML
WuM
MoonRT
2000 Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J Cell Biol 148 519 530
52. TilneyLG
PortnoyDA
1989 Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol 109 1597 1608
53. HolmesKC
PoppD
GebhardW
KabschW
1990 Atomic model of the actin filament. Nature 347 44 49
54. PollardTD
BlanchoinL
MullinsRD
2000 Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29 545 576
55. PollardTD
1986 Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. J Cell Biol 103 2747 2754
56. KovalM
PreiterK
AdlesC
StahlPD
SteinbergTH
1998 Size of IgG-opsonized particles determines macrophage response during internalization. Exp Cell Res 242 265 273
57. ChampionJA
WalkerA
MitragotriS
2008 Role of particle size in phagocytosis of polymeric microspheres. Pharm Res 25 1815 1821
58. FinleyKR
BermanJ
2005 Microtubules in Candida albicans hyphae drive nuclear dynamics and connect cell cycle progression to morphogenesis. Eukaryot Cell 4 1697 1711
59. NgLG
HsuA
MandellMA
RoedigerB
HoellerC
2008 Migratory dermal dendritic cells act as rapid sensors of protozoan parasites. PLoS Pathog 4 e1000222 doi:10.1371/journal.ppat.1000222
60. GreenPJ
FeiziT
StollMS
ThielS
PrescottA
1994 Recognition of the major cell surface glycoconjugates of Leishmania parasites by the human serum mannan-binding protein. Mol Biochem Parasitol 66 319 328
61. AkilovOE
KasuboskiRE
CarterCR
McDowellMA
2007 The role of mannose receptor during experimental leishmaniasis. J Leukoc Biol 81 1188 1196
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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