Circulating human rotavirus specific CD4 T cells identified with a class II tetramer express the intestinal homing receptors α4β7 and CCR9

Virology

Volumn 452-453, Issue , 2014, Pages 191-201

  Parra, Miguel ^a   Herrera, Daniel ^a   Calvo Calle, J Mauricio ^b   Stern, Lawrence J ^b   Parra López, Carlos A ^c   Butcher, Eugene ^d   Franco, Manuel ^a   Angel, Juana ^a  

^a PONTIFICIA UNIVERSIDAD JAVERIANA   (Colombia)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Intestinal homing receptors; MHC class II tetramers; Rotavirus (RV); T cells

Indexed keywords

INTESTINAL HOMING RECEPTORS; MHC CLASS II TETRAMERS; ROTAVIRUS (RV); T CELLS;

ADOLESCENT; ADULT; CD4-POSITIVE T-LYMPHOCYTES; CHILD; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; INTEGRINS; INTESTINES; MALE; RECEPTORS, CCR; RECEPTORS, VIRUS; ROTAVIRUS; ROTAVIRUS INFECTIONS; SPECIES SPECIFICITY; VIRAL PROTEINS; YOUNG ADULT;

EID: 84893582726     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.01.014     Document Type: Article

References (42)

1. Angel J., Franco M.A., Greenberg H.B. Rotavirus immune responses and correlates of protection. Curr. Opin. Virol. 2012, 2:419-425.
2. Baños D.M., Lopez S., Arias C.F., Esquivel F.R. Identification of a T-helper cell epitope on the rotavirus VP6 protein. J. Virol. 1997, 71:419-426.
3. Blutt S.E., Kirkwood C.D., Parreno V., Warfield K.L., Ciarlet M., Estes M.K., Bok K., Bishop R.F., Conner M.E. Rotavirus antigenaemia and viraemia: a common event?. Lancet 2003, 362:1445-1449.
4. Blutt S.E., Miller A.D., Salmon S.L., Metzger D.W., Conner M.E. IgA is important for clearance and critical for protection from rotavirus infection. Mucosal Immunol. 2012, 5:712-719.
5. Butcher E.C., Picker L.J. Lymphocyte homing and homeostasis. Science 1996, 272:60-66.
6. Calvo-Calle J.M., Strug I., Nastke M.-D., Baker S.P., Stern L.J. Human CD4+ T cell epitopes from vaccinia virus induced by vaccination or infection. PLoS Pathog. 2007, 3:1511-1529.
7. Cameron T.O., Norris P.J., Patel A., Moulon C., Rosenberg E.S., Mellins E.D., Wedderburn L.R., Stern L.J. Labeling antigen-specific CD4(+) T cells with class II MHC oligomers. J. Immunol. Methods 2002, 268:51-69.
8. Chicz R.M., Urban R.G., Lane W.S., Gorga J.C., Stern L.J., Vignali D.A., Strominger J.L. Predominant naturally processed peptides bound to HLA-DR1 are derived from MHC-related molecules and are heterogeneous in size. Nature 1992, 358:764-768.
9. Danke N.A., Kwok W.W. HLA class II-restricted CD4+ T cell responses directed against influenza viral antigens postinfluenza vaccination. J. Immunol. 2003, 171:3163-3169.
10. Franco M.A., Angel J., Greenberg H.B. Immunity and correlates of protection for rotavirus vaccines. Vaccine 2006, 24:2718-2731.
11. Franco M.A., Greenberg H.B. Immunity to rotavirus in T cell deficient mice. Virology 1997, 238:169-179.
12. Gattinoni L., Lugli E., Ji Y., Pos Z., Paulos C.M., Quigley M.F., Almeida J.R., Gostick E., Yu Z., Carpenito C., Wang E., Douek D.C., Price D.A., June C.H., Marincola F.M., Roederer M., Restifo N.P. A human memory T cell subset with stem cell-like properties. Nat. Med. 2011, 17:1290-1297.
13. Gilger M.A., Matson D.O., Conner M.E., Rosenblatt H.M., Finegold M.J., Estes M.K. Extraintestinal rotavirus infections in children with immunodeficiency. J. Pediatr. 1992, 120:912-917.
14. Glass R.I., Parashar U., Patel M., Tate J., Jiang B., Gentsch J. The control of rotavirus gastroenteritis in the United States. Trans. Am. Clin. Climatol. Assoc. 2012, 123:36-53.
15. Greenbaum J., Sidney J., Chung J., Brander C., Peters B., Sette A. Functional classification of class II human leukocyte antigen (HLA) molecules reveals seven different supertypes and a surprising degree of repertoire sharing across supertypes. Immunogenetics 2011, 63:325-335.
16. Hammer J., Bono E., Gallazzi F., Belunis C., Nagy Z., Sinigaglia F. Precise prediction of major histocompatibility complex class II-peptide interaction based on peptide side chain scanning. J. Exp. Med. 1994, 180:2353-2358.
17. Honeyman M.C., Stone N.L., Falk B.A., Nepom G., Harrison L.C. Evidence for molecular mimicry between human T cell epitopes in rotavirus and pancreatic islet autoantigens. J. Immunol. 2010, 184:2204-2210.
18. Jaimes M.C., Rojas O.L., González A.M., Cajiao I., Charpilienne A., Pothier P., Kohli E., Greenberg H.B., Franco M.A., Angel J. Frequencies of virus-specific CD4(+) and CD8(+) T lymphocytes secreting gamma interferon after acute natural rotavirus infection in children and adults. J. Virol. 2002, 76:4741-4749.
19. Kwok W.W., Yang J., James E., Bui J., Huston L., Wiesen A.R., Roti M. The anthrax vaccine adsorbed vaccine generates protective antigen (PA)-Specific CD4+ T cells with a phenotype distinct from that of naive PA T cells. Infect. Immun. 2008, 76:4538-4545.
20. Laughlin E.M., Miller J.D., James E., Fillos D., Ibegbu C.C., Mittler R.S., Akondy R., Kwok W., Ahmed R., Nepom G. Antigen-specific CD4+ T cells recognize epitopes of protective antigen following vaccination with an anthrax vaccine. Infect. Immun. 2007, 75:1852-1860.
21. Lissina A., Ladell K., Skowera A., Clement M., Edwards E., Seggewiss R., van den Berg H.A., Gostick E., Gallagher K., Jones E., Melenhorst J.J., Godkin A.J., Peakman M., Price D.A., Sewell A.K., Wooldridge L. Protein kinase inhibitors substantially improve the physical detection of T-cells with peptide-MHC tetramers. J. Immunol. Methods 2009, 340:11-24.
22. Mavigner M., Cazabat M., Dubois M., L'faqihi F.-E., Requena M., Pasquier C., Klopp P., Amar J., Alric L., Barange K., Vinel J.-P., Marchou B., Massip P., Izopet J., Delobel P. Altered CD4+ T cell homing to the gut impairs mucosal immune reconstitution in treated HIV-infected individuals. J. Clin. Invest. 2012, 122:62-69.
23. Mesa M.C., Gutiérrez L., Duarte-Rey C., Angel J., Franco M.A. A TGF-beta mediated regulatory mechanism modulates the T cell immune response to rotavirus in adults but not in children. Virology 2010, 399:77-86.
24. Nastke M.-D., Becerra A., Yin L., Dominguez-Amorocho O., Gibson L., Stern L.J., Calvo-Calle J.M. Human CD4+ T Cell Response to Human Herpesvirus 6. J. Virol. 2012, 86:4776-4792.
25. Nepom G.T. MHC class II tetramers. J. Immunol. 2012, 188:2477-2482.
26. Parra-López C., Calvo-Calle J.M., Cameron T.O., Vargas L.E., Salazar L.M., Patarroyo M.E., Nardin E., Stern L.J. Major histocompatibility complex and T cell interactions of a universal T cell epitope from Plasmodium falciparum circumsporozoite protein. J. Biol. Chem. 2006, 281:14907-14917.
27. Quah B.J.C., Parish C.R. The Use of Carboxyfluorescein Diacetate Succinimidyl Ester (CFSE) to Monitor Lymphocyte Proliferation. J. Vis. Exp. 2010, 44:e2259. 10.3791/2259.
28. Quah B.J.C., Warren H.S., Parish C.R. Monitoring lymphocyte proliferation in vitro and in vivo with the intracellular fluorescent dye carboxyfluorescein diacetate succinimidyl ester. Nat. Protoc. 2007, 2:2049-2056.
29. Roche P.A., Cresswell P. High-affinity binding of an influenza hemagglutinin-derived peptide to purified HLA-DR. J. Immunol. 1990, 144:1849-1856.
30. Rojas O.L., Caicedo L., Guzmán C., Rodríguez L.-S., Castañeda J., Uribe L., Andrade Y., Pinzón R., Narváez C.F., Lozano J.M., De Vos B., Franco M.A., Angel J. Evaluation of circulating intestinally committed memory B cells in children vaccinated with attenuated human rotavirus vaccine. Viral Immunol. 2007, 20:300-311.
31. Rojas O.L., González A.M., González R., Pérez-Schael I., Greenberg H.B., Franco M.A., Angel J. Human rotavirus specific T cells: quantification by ELISPOT and expression of homing receptors on CD4+ T cells. Virology 2003, 314:671-679.
32. Roti M., Yang J., Berger D., Huston L., James E.A., Kwok W.W. Healthy human subjects have CD4+ T cells directed against H5N1 influenza virus. J. Immunol. 2008, 180:1758-1768.
33. Rott L.S., Rosé J.R., Bass D., Williams M.B., Greenberg H.B., Butcher E.C. Expression of mucosal homing receptor alpha4beta7 by circulating CD4+ cells with memory for intestinal rotavirus. J. Clin. Invest. 1997, 100:1204-1208.
34. Sallusto F., Lanzavecchia A. Heterogeneity of CD4+ memory T cells: functional modules for tailored immunity. Eur. J. Immunol. 2009, 39:2076-2082.
35. Schuler M.M., Nastke M.-D., Stevanovikć S. SYFPEITHI: database for searching and T-cell epitope prediction. Methods Mol. Biol. 2007, 409:75-93.
36. Sigmundsdottir H., Butcher E.C. Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat. Immunol. 2008, 9:981-987.
37. Sturniolo T., Bono E., Ding J., Raddrizzani L., Tuereci O., Sahin U., Braxenthaler M., Gallazzi F., Protti M.P., Sinigaglia F., Hammer J. Generation of tissue-specific and promiscuous HLA ligand databases using DNA microarrays and virtual HLA class II matrices. Nat. Biotechnol. 1999, 17:555-561.
38. Tate J.E., Burton A.H., Boschi-Pinto C., Steele A.D., Duque J., Parashar U.D. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect. Dis. 2012, 12:136-141.
39. Vollers S.S., Stern L.J. Class II major histocompatibility complex tetramer staining: progress, problems, and prospects. Immunology 2008, 123:305-313.
40. Waldrop S.L., Davis K.A., Maino V.C., Picker L.J. Normal human CD4+ memory T cells display broad heterogeneity in their activation threshold for cytokine synthesis. J. Immunol. 1998, 161:5284-5295.
41. Waldrop S.L., Pitcher C.J., Peterson D.M., Maino V.C., Picker L.J. Determination of antigen-specific memory/effector CD4+ T cell frequencies by flow cytometry: evidence for a novel, antigen-specific homeostatic mechanism in HIV-associated immunodeficiency. J. Clin. Invest. 1997, 99:1739-1750.
42. Zhao W., Pahar B., Sestak K. Identification of Rotavirus VP6-Specific CD4+ T Cell Epitopes in a G1P[8] Human Rotavirus-Infected Rhesus Macaque. Virology (Auckl.) 2008, 1:9-15.