Prokineticin receptor identified by phage display is an entry receptor for Trypanosoma cruzi into mammalian cells

Parasitology Research

Volumn 114, Issue 1, 2015, Pages 155-165

  Khusal, K G ^a   Tonelli, R R ^b   Mattos, E C ^a   Soares, C O ^a   Di Genova, B M ^b   Juliano, M A ^b   Urias, U ^a   Colli, W ^a   Alves, M J M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

iRNA; Phage display; Prokineticin 2 receptor; T. cruzi invasion

Indexed keywords

GLYCOPROTEIN; GROWTH FACTOR RECEPTOR; PROKINETICIN 2 RECEPTOR; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; PROKR2 PROTEIN, HUMAN; RECEPTOR;

ANIMAL CELL; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CELL INVASION; DNA SEQUENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOST CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOLOCALIZATION; IMMUNOPRECIPITATION; MAMMAL CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; PEPTIDE SYNTHESIS; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; TRYPANOSOMA CRUZI; WESTERN BLOTTING; ANIMAL; BACTERIOPHAGE; CELL LINE; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

MAMMALIA; TRYPANOSOMA CRUZI;

ANIMALS; BACTERIOPHAGES; BINDING SITES; CELL LINE; CONSERVED SEQUENCE; GLYCOPROTEINS; HUMANS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PEPTIDE; TRYPANOSOMA CRUZI;

EID: 84938901272     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-014-4172-6     Document Type: Article

References (60)

1. Abreu AP, Noel SD, Xu S, Carroll RS, Latronico AC, Kaiser UB (2012) Evidence of the importance of the first intracellular loop of prokineticin receptor 2 in receptor function. Mol Endocrinol 26:1417–1427
2. Abuin G, Colli W, De Souza W, Alves MJM (1989) A surface antigen of Trypanosoma cruzi involved in cell invasion (Tc-85) is heterogeneous in expression and molecular constitution. Mol Biochem Parasitol 35:229–238
3. Almeida-de-Faria M, Freymüller E, Colli W, Alves MJM (1999) Trypanosoma cruzi: characterization of an intracellular epimastigote-like form. Exp Parasitol 92:263–274
4. Alves MJM, Colli W (2008) Role of the gp85/trans-sialidase superfamily of glycoproteins in the interaction of Trypanosoma cruzi with host structures. Mol Mech of Parasite Invasion, 47:58–69
5. Andrews NA, Colli W (1982) Adhesion and interiorization of Trypanosoma cruzi in mammalian cells. J Protozool 29:264–269
6. Atwood JA, Weatherly DB, Minning TA, Bundy B, Cavola C, Opperdoes FR, Orlando R, Tarleton RL (2005) The Trypanosoma cruzi proteome. Science 309:473–476
7. Bombeiro A, Goncalves L, Penha-Goncalves C, Marinho C, D’Imperio Lima M, Chadi G, Alvarez J (2012) IL-12p40 deficiency leads to uncontrolled Trypanosoma cruzi dissemination in the spinal cord resulting in neuronal death and motor dysfunction. PLoS One 7:e49022
8. Calvet CM, Toma L, De Souza FR, Meirelles MN, Pereira MCS (2003) Heparan sulfate proteoglycans mediate the invasion of cardiomyocytes by Trypanosoma cruzi. J Eukaryot Microbiol 50:97–103
9. Caradonna K, Burleigh B (2011) Mechanisms of host cell invasion by Trypanosoma cruzi. Adv Parasitol 76:33–61
10. Caradonna KL, Engel JC, Jacobi D, Lee CH, Burleigh BA (2013) Host metabolism regulates intracellular growth of Trypanosoma cruzi. Cell Host Microbe 13:108–117
11. Cella N, Contreras A, Latha K, Rosen JM, Zhang M (2006) Maspin is physically associated with {beta}1 integrin regulating cell adhesion in mammary epithelial cells. FASEB J 20:1510–1512
12. Cole LW, Sidis Y, Zhang C, Quinton R, Plummer L, Pignatelli D, Hughes VA, Dwyer AA, Raivio T, Hayes FJ, Seminara SB, Huot C, Alos N, Speiser P, Takeshita A, VanVliet G, Pearce S, Crowley WF Jr, Zhou Q-Y, Pitteloud N (2008) Mutations in prokineticin 2 and prokineticin receptor 2 genes in human gonadotrophin-releasing hormone deficiency: molecular genetics and clinical spectrum. J Clin Endocrinol Metab 93:3551–3559
13. Cordova E, Maiolo E, Corti M, Orduna T (2010) Neurological manifestations of Chagas’ disease. Neurol Res 32:238–244
14. Cortez C, Yoshida N, Bahia D, Sobreira TJ (2012) Structural basis of the interaction of a Trypanosoma cruzi surface molecule implicated in oral infection with host cells and gastric mucin. PLoS One 7:e42153
15. da Mata JR, Camargos E, Chiari E, Machado CR (2000) Trypanosoma cruzi infection and the rat central nervous system: proliferation of parasites in astrocytes and the brain reaction to parasitism. Brain res Bull 53:153–162
16. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran A-N, Ghedin E, Worthey EA, Delcher AL, Blandin G, Westenberger SJ, Caler E, Cerqueira GC, Branche C, Haas B, Anupama A, Arner E, Aslund L, Attipoe P, Bontempi E, Bringaud F, Burton P, Cadag E, Campbell DA, Carrington M, Crabtree J, Darban H, da Silveira JF, de Jong P, Edwards K, Englund PT, Fazelina G, Feldblyum T, Ferella M, Frasch AC, Gull K, Horn D, Hou L, Huang Y, Kindlund E, Klingbeil M, Kluge S, Koo H, Lacerda D, Levin MJ, Lorenzi H, Louie T, Machado CR, McCulloch R, McKenna A, Mizuno Y, Mottram JC, Nelson S, Ochaya S, Osoegawa K, Pai G, Parsons M, Pentony M, Pettersson U, Pop M, Ramirez JL, Rinta J, Robertson L, Salzberg SL, Sanchez DO, Seyler A, Sharma R, Shetty J, Simpson AJ, Sisk E, Tammi MT, Tarleton R, Teixeira S, Van Aken S, Vogt C, Ward PN, Wickstead B, Wortman J, White O, Fraser CM, Stuart KD, Andersson B (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas’ Disease. Science 309:409–415
17. Feldmesser E, Olender T, Khen M, Yanai I, Ophir R, Lancet D (2006) Widespread ectopic expression of olfactory receptor genes. BMC Genomics 7:121
18. Fernandes MC, Andrews NW (2012) Host cell invasion by Trypanosoma cruzi: a unique strategy that promotes persistence. FEMS Microbiol Rev 36:734–747
19. Fernandes MC, Cortez M, Flannery AR, Tam C, Mortara RA, Andrews NW (2011) Trypanosoma cruzi subverts the sphingomyelinase-mediated plasma membrane repair pathway for cell invasion. J Exp Med 208:909–921
20. Flegel C, Manteniotis S, Osthold S, Hatt H, Gisselmann G (2013) Expression profile of ectopic olfactory receptors determined by deep sequencing. PLoS One 8:e55368
21. Freitas LM, dos Santos SL, Rodrigues-Luiz GF, Mendes TA, Rodrigues TS, Gazzinelli RT, Teixeira SMR, Fujiwara RT, Bartholomeu DC (2011) Genomic analyses, gene expression and antigenic profile of the trans-sialidase superfamily of Trypanosoma cruzi reveal an undetected level of complexity. PLoS One 6:e25914
22. Genovesio A, Giardini M, Kwon Y, de Macedo Dossin F, Choi S, Kim N, Kim H, Jung S, Schenkman S, Almeida I, Emans N, Freitas-Junior L (2011) Visual genome-wide RNAi screening to identify human host factors required for Trypanosoma cruzi infection. PLoS One 6:e19733
23. Giordano R, Chamas R, Veiga SS, Colli W, Alves MJM (1994) An acidic component of the heterogeneous Tc-85 protein family from surface of Trypanosoma cruzi is a laminin binding glycoprotein. Mol Biochem Parasitol 65:85–94
24. Giordano R, Fouts DL, Tewari DS, Colli W, Manning JE, Alves MJM (1999) Cloning of a surface membrane glycoprotein specific for the infective form of Trypanosoma cruzi having adhesive properties to laminin. J Biol Chem 274:3461–3468
25. Giordano RJ, Cardo-Vila M, Lahdenranta J, Pasqualini R, Arap W (2001) Biopanning and rapid analysis of selective interactive ligands. Nat Med 7:1249–1253
26. Gonçalves MF, Umezawa ES, Katzin AM, de Souza W, Alves MJM, Zingales B, Colli W (1991) Trypanosoma cruzi: shedding of surface antigens as membrane vesicles. Exp Parasitol 72:43–53
27. Guilini C, Urayama K, Turkeri G, Dedeoglu DB, Kurose H, Messaddeq N, Nebigil CG (2010) Divergent roles of prokineticin receptors in the endothelial cells: angiogenesis and fenestration. Am J Physiol Heart Circ Physiol 298:H844–H852
28. Hidalgo ME, Hernandez R, Keene WE, McKerrow JH, Orozco E (1990) Direct relation between secretion of proteolytic enzymes and virulence in Entamoeba histolytica. Arch Invest Med (Mex) 21(Suppl 1):133–138
29. Kahn SJ, Nguyen D, Norsen J, Wleklinski M, Granston T, Kahn M (1999) Trypanosoma cruzi: monoclonal antibodies to the surface glycoprotein superfamily differentiate subsets of the 85-kDa surface glycoproteins and confirm simultaneous expression of variant 85-kDa surface glycoproteins. Exp Parasitol 92:48–56
30. Kisliouk T, Levy N, Hurwitz A, Meidan R (2003) Presence and regulation of endocrine gland vascular endothelial growth factor/prokineticin-1 and Its receptors in ovarian cells. J Clin Endocrinol Metab 88:3700–3707
31. Köhler G, Milstein C (1975) Continuous cultures of fused cells secreting antibody of predefined specificity. Neture 256:495–497
32. Lin DC-H, Bullock CM, Ehlert FJ, Chen J-L, Tian H, Zhou Q-Y (2002) Identification and molecular characterization of two closely related G protein-coupled receptors activated by prokineticins/endocrine gland vascular endothelial growth factor. J Biol Chem 277:1927619280
33. Magdesian MH, Giordano RJ, Ulrich H, Juliano MA, Juliano L, Schumacher RI, Colli W, Alves MJM (2001) Infection by Trypanosoma cruzi identification of a parasite ligand and its host cell receptor. J Biol Chem 276:19382–19389
34. Magdesian MH, Tonelli RR, Fessel MR, Silveira MS, Schumacher RI, Linden R, Colli W, Alves MJM (2007) A conserved domain of the gp85/trans-sialidase family activates host cell extracellular signal-regulated kinase and facilitates Trypanosoma cruzi infection. Exp Cell Res 313:210–218
35. Marroquin-Quelopana M, Oyama S Jr, Pertinhez TA, Spisni A, Juliano MA, Juliano L, Colli W, Alves MJM (2004) Modeling the Trypanosoma cruzi Tc85-11 protein and mapping the laminin-binding site. Biochem Biophys Res Commun 325:612–618
36. Marsango S, Bonaccorsi di Patti MC, Barra D, Miele R (2011) Evidence that prokineticin receptor 2 exists as a dimer in vivo. Cell Mol Life Sci 68:2919–2929
37. Moncada D, Yu Y, Keller K, Chadee K (2000) Entamoeba histolytica cysteine proteinases degrade human colonic mucin and alter its function. Arch Med Res 31:S224–S225
38. Monnier C, Dode C, Fabre L, Teixeira L, Labesse G, Pin J-P, Hardelin J-P, Rondard P (2009) PROKR2 missense mutations associated with Kallmann syndrome impair receptor signalling activity. Hum Mol Genet 18:75–81
39. Morocoima A, Socorro G, Avila R, Hernandez A, Merchan S, Ortiz D, Primavera G, Chique J, Herrera L, Urdaneta-Morales S (2012) Trypanosoma cruzi: experimental parasitism in the central nervous system of albino mice. Parasitol Res 111:2099–2107
40. Nagajyothi F, Machado F, Burleigh B, Jelicks L, Scherer P, Mukherjee S, Lisanti M, Weiss L, Garg N, Tanowitz H (2012) Mechanisms of Trypanosoma cruzi persistence in Chagas disease. Cell Microbiol 14:634–643
41. Nde PN, Lima MF, Johnson CA, Pratap S, Villalta F (2012) Regulation and use of the extracellular matrix by Trypanosoma cruzi during early infection. Front Immunol 3:337
42. Nebigil C (2009) Prokineticin receptors in cardiovascular function: foe or friend? Trends Cardiovas Med 19:55–60
43. Ngan E, Tam P (2008) Prokineticin-signaling pathway. Int J Biochem Cell Biol 40:16791684
44. Oppezzo P, Obal G, Baraibar MA, Pritsch O, Alzari PM, Buschiazzo A (2011) Crystal structure of an enzymatically inactive trans-sialidase-like lectin from Trypanosoma cruzi: the carbohydrate binding mechanism involves residual sialidase activity. Biochim Biophys Acta 1814:1154–1161
45. Ouaissi MA, Afchain D, Capron A, Grimaud JA (1984) Fibronectin receptors on Trypanosoma cruzi trypomastigotes and their biological function. Nature 308:380–382
46. Pablos LM, Osuna A (2012) Conserved regions as markers of different patterns of expression and distribution of the mucin-associated surface proteins of Trypanosoma cruzi. Infect Immun 80:169–174
47. Peng Z, Tang Y, Luo H, Jiang F, Yang J, Sun L, Li J-D (2011) Disease-causing mutation in PKR2 receptor reveals a critical role of positive charges in the second intracellular loop for G-protein coupling and receptor trafficking. J Biol Chem 286:16615–16622
48. Rachid MA, Teixeira AL, Barcelos LS, Machado CR, Chiari E, Tanowitz HB, Camargos ER, Teixeira MM (2010) Role of endothelin receptors in the control of central nervous system parasitism in Trypanosoma cruzi infection in rats. J Neuroimmunol 220:64–68
49. Schioth H, Fredriksson R (2005) The GRAFS classification system of G-protein coupled receptors in comparative perspective. Gen Comp Endocrinol 142:94–101
50. Schneider C, Rasband W, Eliceiri K (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
51. Silva AA, Rofle E, Santiago H, Marino AP, Kroll-Palhares K, Teixeira MM, Gazzinelli RT, Lannes-Vieira J (2007) Trypanosoma cruzi -triggered meningoencephalitis is a CCR1/CCR5- independent inflammatory process. J Neuroimmunol 184:156–163
52. Smith GP (1985) Filamentous fusion phage: novel expression vectors that display antigens on the virion surface. Science 228:1315–1317
53. Todeschini AR, Dias WB, Girard MF, Wieruszeski J-M, Mendonca-Previato L, Previato JO (2004) Enzymatically inactive trans-sialidase from Trypanosoma cruzi binds sialyl and βgalactopyranosyl residues in a sequential ordered mechanism. J Biol Chem 279:5323–5328
54. Tonelli RR, Colli W, Alves MJM (2012) Selection of binding targets in parasites using phage-display and aptamer libraries in vivo and in vitro. Front Immunol 3:419
55. Tonelli RR, Giordano RJ, Barbu EM, Torrecilhas AC, Kobayashi GS, et al. (2010) Role of the gp85/Trans-Sialidases in Trypanosoma cruzi tissue tropism: preferential binding of a conserved peptide motif to the vasculature in vivo. PLoS Negl Trop Dis 4(11): e864
56. Torrecilhas ACT, Schumacher RI, Alves MJM, Colli W (2012) Vesicles as carriers of virulence factors in parasitic protozoan diseases. Microbes Infect 14:1465–1474
57. Tzraskowski B, Latek D, Yuan S, Ghoshdastider U, Debinski A, Filipek S (2012) Action of molecular switches in GPCRs- Theoretical and experimental studies. Curr Med Chem 19:1090–1109
58. Velge P, Ouaissi MA, Cornette J, Afchain D, Capron A (1988) Identification and isolation of Trypanosoma cruzi trypomastigote collagen-binding proteins: possible role in cell-parasite interaction. Parasitology 97:255–268
59. Ward HD, Keusch GT, Pereira ME (1990) Induction of a phosphomannosyl binding lectin activity in Giardia. BioEssays 12:211–215
60. Weinkauf C, Salvador R, Pereira Perrin M (2011) Neurotrophin receptor TrkC is an entry receptor for Trypanosoma cruzi in neural, glial, and epithelial cells. Infect Immun 79:40814087