Lymphangiogenesis and lymphatic remodeling induced by filarial parasites: Implications for pathogenesis

PLoS Pathogens

Volumn 5, Issue 12, 2009, Pages

  Bennuru, Sasisekhar ^a   Nutman, Thomas B ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCEIN ISOTHIOCYANATE DEXTRAN; MATRIX METALLOPROTEINASE; PARASITE ANTIGEN; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; GELATINASE A; INTERSTITIAL COLLAGENASE;

ARTICLE; CELL DIFFERENTIATION; CELL INTERACTION; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FILARIA; GENE EXPRESSION; HUMAN; HUMAN CELL; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; LYMPHATIC FILARIASIS; MICROFILARIA; NONHUMAN; PARASITE; PATHOGENESIS; PROTEIN EXPRESSION; UPREGULATION; BIOSYNTHESIS; CELL SEPARATION; CONFOCAL MICROSCOPY; DNA MICROARRAY; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; PARASITOLOGY; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

MURINAE;

CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; ELEPHANTIASIS, FILARIAL; ENDOTHELIAL CELLS; FLOW CYTOMETRY; GENE EXPRESSION; HUMANS; LYMPHANGIOGENESIS; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 2; MICROSCOPY, CONFOCAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TISSUE INHIBITOR OF METALLOPROTEINASE-2;

EID: 74549138186     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000688     Document Type: Article

References (54)

1. Rajan TV (1998) A hypothesis for the tissue specificity of nematode parasites. Exp Parasitol 89: 140-142.
2. Connor DH, Palmieri JR, Gibson DW (1986) Pathogenesis of lymphatic filariasis in man. Z Parasitenkd 72: 13-28.
3. Lichtenberg F (1957) The early phase of endemic bancroftian filariasis in the male; pathological study. J Mt Sinai Hosp N Y 24: 983-1000.
4. Klei TR, Enright FM, Blanchard DP, Uhl SA (1981) Specific hypo-responsive granulomatous tissue reactions in Brugia pahangi-infected jirds. Acta Trop 38: 267-276.
5. Nutman TB, Kumaraswami V, Pao L, Narayanan PR, Ottesen EA (1987) An analysis of in vitro B cell immune responsiveness in human lymphatic filariasis. J Immunol 138: 3954-3959.
6. Ottesen EA (1980) Immunopathology of lymphatic filariasis in man. Springer Seminars in Immunopathology 2: 373-385.
7. Piessens WF, McGreevy PB, Piessens PW, McGreevy M, Koiman I, et al. (1980) Immune responses in human infections with Brugia malayi: specific cellular unresponsiveness to filarial antigens. J Clin Invest 65: 172-179.
8. Nelson FK, Greiner DL, Shultz LD, Rajan TV (1991) The immunodeficient scid mouse as a model for human lymphatic filariasis. J Exp Med 173: 659-663.
9. Vincent AL, Vickery AC, Lotz MJ, Desai U (1984) The lymphatic pathology of Brugia pahangi in nude (athymic) and thymic mice C3H/HeN. J Parasitol 70: 48-56.
10. Vickery AC, Albertine KH, Nayar JK, Kwa BH (1991) Histopathology of Brugia malayi-infected nude mice after immune-reconstitution. Acta Trop 49: 45-55.
11. Vickery AC, Vincent AL, Sodeman WA, Jr. (1983) Effect of immune reconstitution on resistance to Brugia pahangi in congenitally athymic nude mice. J Parasitol 69: 478-485.
12. Freedman DO, de Almeido Filho PJ, Besh S, Maia e Silva MC, Braga C, et al. (1995) Abnormal lymphatic function in presymptomatic bancroftian filariasis. J Infect Dis 171: 997-1001.
13. Freedman DO, de Almeida Filho PJ, Besh S, Maia e Silva MC, Braga C, et al. (1994) Lymphoscintigraphic analysis of lymphatic abnormalities in symptomatic and asymptomatic human filariasis. J Infect Dis 170: 927-933.
14. Shenoy RK, Suma TK, Kumaraswami V, Rahmah N, Dhananjayan G, et al. (2007) Preliminary findings from a cross-sectional study on lymphatic filariasis in children, in an area of India endemic for Brugia malayi infection. Ann Trop Med Parasitol 101: 205-213.
15. Amaral F, Dreyer G, Figueredo-Silva J, Noroes J, Cavalcanti A, et al. (1994) Live adult worms detected by ultrasonography in human Bancroftian filariasis. Am J Trop Med Hyg 50: 753-757.
16. Dreyer G, Amaral F, Noroes J, Medeiros Z (1994) Ultrasonographic evidence for stability of adult worm location in bancroftian filariasis. Trans R Soc Trop Med Hyg 88: 558.
17. Dreyer G, Santos A, Noroes J, Amaral F, Addiss D (1998) Ultrasonographic detection of living adult Wuchereria bancrofti using a 3.5-MHz transducer. Am J Trop Med Hyg 59: 399-403.
18. Jungmann P, Figueredo-Silva J, Dreyer G (1991) Bancroftian lymphadenopathy: a histopathologic study of fifty-eight cases from northeastern Brazil. Am J Trop Med Hyg 45: 325-331.
19. Dreyer G, Noroes J, Addiss D, Santos A, Medeiros Z, et al. (1999) Bancroftian filariasis in a paediatric population: an ultrasonographic study. Trans R Soc Trop Med Hyg 93: 633-636.
20. Dreyer G, Noroes J, Figueredo-Silva J, Piessens WF (2000) Pathogenesis of lymphatic disease in bancroftian filariasis: a clinical perspective. Parasitol Today 16: 544-548.
21. Rao UR, Zometa CS, Vickery AC, Kwa BH, Nayar JK, et al. (1996) Effect of Brugia malayi on the growth and proliferation of endothelial cells in vitro. J Parasitol 82: 550-556.
22. Freedman DO, Ottesen EA (1988) Eggs of Schistosoma mansoni stimulate endothelial cell proliferation in vitro. J Infect Dis 158: 556-562.
23. Loeffler DA, Lundy SK, Singh KP, Gerard HC, Hudson AP, et al. (2002) Soluble egg antigens from Schistosoma mansoni induce angiogenesis-related processes by up-regulating vascular endothelial growth factor in human endothelial cells. J Infect Dis 185: 1650-1656.
24. Alitalo K, Tammela T, Petrova TV (2005) Lymphangiogenesis in development and human disease. Nature 438: 946-953.
25. Debrah AY, Mand S, Marfo-Debrekyei Y, Batsa L, Pfarr K, et al. (2009) Reduction in levels of plasma vascular endothelial growth factor-A and improvement in hydrocele patients by targeting endosymbiotic Wolbachia sp. in Wuchereria bancrofti with doxycycline. Am J Trop Med Hyg 80: 956-963.
26. Debrah AY, Mand S, Specht S, Marfo-Debrekyei Y, Batsa L, et al. (2006) Doxycycline reduces plasma VEGF-C/sVEGFR-3 and improves pathology in lymphatic filariasis. PLoS Pathog 2: e92. doi:10.1371/journal.ppat.0020092.
27. Debrah AY, Mand S, Toliat MR, Marfo-Debrekyei Y, Batsa L, et al. (2007) Plasma vascular endothelial growth Factor-A (VEGF-A) and VEGF-A gene polymorphism are associated with hydrocele development in lymphatic filariasis. Am J Trop Med Hyg 77: 601-608.
28. Esterre P, Plichart C, Huin-Blondey MO, Nguyen LN (2005) Soluble cellular adhesion molecules, selectins, VEGF and endothelin-1 in patients with Wuchereria bancrofti infection and association with clinical status. Parasite Immunol 27: 9-16.
29. Leak LV (1985) Interaction of mesothelium to intraperitoneal stimulation: II Formation of granulation tissue. Am J Anat 173: 171-183.
30. Alitalo K, Carmeliet P (2002) Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell 1: 219-227.
31. Ingber DE, Folkman J (1989) How does extracellular matrix control capillary morphogenesis? Cell 58: 803-805.
32. Montesano R (1986) Cell-extracellular matrix interactions in morphogenesis: an in vitro approach. Experientia 42: 977-985.
33. Bjorndahl M, Cao R, Nissen LJ, Clasper S, Johnson LA, et al. (2005) Insulin-like growth factors 1 and 2 induce lymphangiogenesis in vivo. Proc Natl Acad Sci U S A 102: 15593-15598.
34. Cao R, Bjorndahl MA, Religa P, Clasper S, Garvin S, et al. (2004) PDGF-BB induces intratumoral lymphangiogenesis and promotes lymphatic metastasis. Cancer Cell 6: 333-345.
35. Chang LK, Garcia-Cardena G, Farnebo F, Fannon M, Chen EJ, et al. (2004) Dose-dependent response of FGF-2 for lymphangiogenesis. Proc Natl Acad Sci U S A 101: 11658-11663.
36. Kubo H, Cao R, Brakenhielm E, Makinen T, Cao Y, et al. (2002) Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea. Proc Natl Acad Sci U S A 99: 8868-8873.
37. Tammela T, Saaristo A, Lohela M, Morisada T, Tornberg J, et al. (2005) Angiopoietin-1 promotes lymphatic sprouting and hyperplasia. Blood 105: 4642-4648.
38. Leak LV, Jones M (1994) Lymphangiogenesis in vitro: formation of lymphatic capillary-like channels from confluent monolayers of lymphatic endothelial cells. In Vitro Cell Dev Biol Anim 30A: 512-518.
39. Kubota Y, Kleinman HK, Martin GR, Lawley TJ (1988) Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol 107: 1589-1598.
40. Djoneidi M, Brodt P (1991) Isolation and characterization of rat lymphatic endothelial cells. Microcirc Endothelium Lymphatics 7: 161-182.
41. Kraling BM, Wiederschain DG, Boehm T, Rehn M, Mulliken JB, et al. (1999) The role of matrix metalloproteinase activity in the maturation of human capillary endothelial cells in vitro. J Cell Sci 112(Pt 10): 1599-1609.
42. Murphy G, Willenbrock F, Crabbe T, O'Shea M, Ward R, et al. (1994) Regulation of matrix metalloproteinase activity. Ann N Y Acad Sci 732: 31-41.
43. Nagase H, Suzuki K, Itoh Y, Kan CC, Gehring MR, et al. (1996) Involvement of tissue inhibitors of metalloproteinases (TIMPS) during matrix metalloproteinase activation. Adv Exp Med Biol 389: 23-31.
44. Moses MA (1997) The regulation of neovascularization of matrix metalloproteinases and their inhibitors. Stem Cells 15: 180-189.
45. Stetler-Stevenson WG, Seo DW (2005) TIMP-2: an endogenous inhibitor of angiogenesis. Trends Mol Med 11: 97-103.
46. Rogers R, Denham DA, Nelson GS, Guy F, Ponnudurai T (1975) Studies with Brugia pahangi. III: Histological changes in the affected lymph nodes of infected cats. Ann Trop Med Parasitol 69: 77-84.
47. Sakamoto M, Meier JL, Folse DS, Ewert A (1985) Perturbation of lymphatic endothelial cells in experimental Brugia malayi infections. Microcirc Endothelium Lymphatics 2: 487-498.
48. Sakamoto M, Shimada M, Fujimaki Y, Ewert A (1988) Degenerative changes in lymphatic endothelium of jirds infected with Brugia pahangi. J Parasitol 74: 731-734.
49. Rogers R, Denham DA (1974) Studies with Brugia pahagi. 7. Changes in lymphatics of injected cats. J Helminthol 48: 213-219.
50. Morchon R, Rodriguez-Barbero A, Velasco S, Lopez-Belmonte J, Simon F (2008) Vascular endothelial cell activation by adult Dirofilaria immitis antigens. Parasitol Int 57: 441-446.
51. Babu S, Blauvelt CP, Kumaraswami V, Nutman TB (2005) Chemokine receptors of T cells and of B cells in lymphatic filarial infection: a role for CCR9 in pathogenesis. J Infect Dis 191: 1018-1026.
52. Bennuru S, Semnani R, Meng Z, Ribeiro JM, Veenstra TD, et al. (2009) Brugia malayi Excreted/Secreted Proteins at the Host/Parasite Interface: Stage- and Gender-Specific Proteomic Profiling. PLoS Negl Trop Dis 3: e410. doi:10.1371/journal.pntd.0000410.
53. Moreno Y, Geary TG (2008) Stage- and Gender-Specific Proteomic Analysis of Brugia malayi Excretory-Secretory Products. PLoS Negl Trop Dis 2: e326.
54. Hussain R, Hamilton RG, Kumaraswami V, Adkinson NF Jr, Ottesen EA (1981) IgE responses in human filariasis. I. Quantitation of filaria-specific IgE. J Immunol 127: 1623-1629.