Differential expression of genes in salivary glands of male Rhipicephalus (Boophilus)microplus in response to infection with Anaplasma marginale

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Zivkovic, Zorica ^a   Esteves, Eliane ^b   Almazán, Consuelo ^c   Daffre, Sirlei ^b   Nijhof, Ard M ^a   Kocan, Katherine M ^d   Jongejan, Frans ^a,e   de la Fuente, José ^d,f  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSIDAD AUTÓNOMA DE TAMAULIPAS   (Mexico)

^d OKLAHOMA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF PRETORIA   (South Africa)

^f INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; FLAGELLIFORM SILK PROTEIN; HISTAMINE BINDING PROTEIN; METALLOTHIONEIN; PROLINE RICH PROTEIN BSTNI SUBFAMILY 3; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ANAPLASMA MARGINALE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE SILENCING; MALE; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN BINDING; PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHIPICEPHALUS; RHIPICEPHALUS MICROPLUS; RNA INTERFERENCE; SALIVARY GLAND; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; UPREGULATION; ANIMAL; CELL LINE; DNA SEQUENCE; EXPRESSED SEQUENCE TAG; GENE EXPRESSION PROFILING; GENE LIBRARY; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; NUCLEIC ACID HYBRIDIZATION; PHYSIOLOGY;

ANAPLASMA MARGINALE; ANAPLASMATACEAE; BOOPHILUS; BOS; BOVINAE; DERMACENTOR VARIABILIS; IXODES SCAPULARIS; IXODIDA; RHIPICEPHALUS; RICKETTSIALES;

ANAPLASMA MARGINALE; ANIMALS; CELL LINE; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENE LIBRARY; HOST-PATHOGEN INTERACTIONS; MALE; NUCLEIC ACID HYBRIDIZATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHIPICEPHALUS; RNA INTERFERENCE; SALIVARY GLANDS; SEQUENCE ANALYSIS, DNA;

EID: 77951230771     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-186     Document Type: Article

References (56)

1. Kocan KM, de la Fuente J, Guglielmone AA, Melendez RD. Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clin Microbiol Rev 2003, 16(4):698-712. 10.1128/CMR.16.4.698-712.2003, 207124, 14557295.
2. Kocan KM, de la Fuente J, Blouin EF, Garcia-Garcia JC. Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host-pathogen adaptations of a tick-borne rickettsia. Parasitology 2004, 129(Suppl):S285-300. 10.1017/S0031182003004700, 15938516.
3. Guerrero FD, Nene VM, George JE, Barker SC, Willadsen P. Sequencing a new target genome: the Boophilus microplus (Acari: Ixodidae) genome project. J Med Entomol 2006, 43(1):9-16. 10.1603/0022-2585(2006)043[0009:SANTGT]2.0.CO;2, 16506442.
4. de Castro JJ. Sustainable tick and tickborne disease control in livestock improvement in developing countries. Vet Parasitol 1997, 71(2-3):77-97. 10.1016/S0304-4017(97)00033-2, 9261972.
5. Kocan KM, Goff WL, Stiller D, Claypool PL, Edwards W, Ewing SA, Hair JA, Barron SJ. Persistence of Anaplasma marginale (Rickettsiales: Anaplasmataceae) in male Dermacentor andersoni (Acari: Ixodidae) transferred successively from infected to susceptible calves. J Med Entomol 1992, 29(4):657-668.
6. Kocan KM, Stiller D, Goff WL, Claypool PL, Edwards W, Ewing SA, McGuire TC, Hair JA, Barron SJ. Development of Anaplasma marginale in male Dermacentor andersoni transferred from parasitemic to susceptible cattle. Am J Vet Res 1992, 53(4):499-507.
7. Chevillon C, Koffi BB, Barre N, Durand P, Arnathau C, de Meeus T. Direct and indirect inferences on parasite mating and gene transmission patterns. Pangamy in the cattle tick Rhipicephalus (Boophilus) microplus. Infect Genet Evol 2007, 7(2):298-304. 10.1016/j.meegid.2006.11.007, 17215171.
8. Macaluso KR, Mulenga A, Simser JA, Azad AF. Differential expression of genes in uninfected and rickettsia-infected Dermacentor variabilis ticks as assessed by differential-display PCR. Infect Immun 2003, 71(11):6165-6170. 10.1128/IAI.71.11.6165-6170.2003, 219596, 14573632.
9. Nene V, Lee D, Kang'a S, Skilton R, Shah T, de Villiers E, Mwaura S, Taylor D, Quackenbush J, Bishop R. Genes transcribed in the salivary glands of female Rhipicephalus appendiculatus ticks infected with Theileria parva. Insect Biochem Mol Biol 2004, 34(10):1117-1128. 10.1016/j.ibmb.2004.07.002, 15475305.
10. Rudenko N, Golovchenko M, Edwards MJ, Grubhoffer L. Differential expression of Ixodes ricinus tick genes induced by blood feeding or Borrelia burgdorferi infection. J Med Entomol 2005, 42(1):36-41. 10.1603/0022-2585(2005)042[0036:DEOIRT]2.0.CO;2, 15691006.
11. de la Fuente J, Kocan KM, Almazan C, Blouin EF. RNA interference for the study and genetic manipulation of ticks. Trends Parasitol 2007, 23(9):427-433. 10.1016/j.pt.2007.07.002, 17656154.
12. Bell-Sakyi L, Zweygarth E, Blouin EF, Gould EA, Jongejan F. Tick cell lines: tools for tick and tick-borne disease research. Trends Parasitol 2007, 23(9):450-457. 10.1016/j.pt.2007.07.009, 17662657.
13. Esteves E, Bastos CV, Zivkovic Z, de La Fuente J, Kocan K, Blouin E, Ribeiro MF, Passos LM, Daffre S. Propagation of a Brazilian isolate of Anaplasma marginale with appendage in a tick cell line (BME26) derived from Rhipicephalus (Boophilus) microplus. Vet Parasitol 2008, 161(1-2):150-3. 10.1016/j.vetpar.2008.12.006, 19150177.
14. Diatchenko L, Lukyanov S, Lau YF, Siebert PD. Suppression subtractive hybridization: a versatile method for identifying differentially expressed genes. Methods Enzymol 1999, 303:349-380. full_text, 10349654.
15. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, et al. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 1996, 93(12):6025-6030. 10.1073/pnas.93.12.6025, 39182, 8650213.
16. Pal U, Li X, Wang T, Montgomery RR, Ramamoorthi N, Desilva AM, Bao F, Yang X, Pypaert M, Pradhan D, et al. TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 2004, 119(4):457-468. 10.1016/j.cell.2004.10.027, 15537536.
17. Ramamoorthi N, Narasimhan S, Pal U, Bao F, Yang XF, Fish D, Anguita J, Norgard MV, Kantor FS, Anderson JF, et al. The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 2005, 436(7050):573-577. 10.1038/nature03812, 16049492.
18. Sukumaran B, Narasimhan S, Anderson JF, DePonte K, Marcantonio N, Krishnan MN, Fish D, Telford SR, Kantor FS, Fikrig E. An Ixodes scapularis protein required for survival of Anaplasma phagocytophilum in tick salivary glands. J Exp Med 2006, 203(6):1507-1517. 10.1084/jem.20060208, 2118316, 16717118.
19. de la Fuente J, Almazan C, Blouin EF, Naranjo V, Kocan KM. Reduction of tick infections with Anaplasma marginale and A. phagocytophilum by targeting the tick protective antigen subolesin. Parasitol Res 2006, 100(1):85-91. 10.1007/s00436-006-0244-6, 16816958.
20. de la Fuente J, Lew A, Lutz H, Meli ML, Hofmann-Lehmann R, Shkap V, Molad T, Mangold AJ, Almazan C, Naranjo V, et al. Genetic diversity of anaplasma species major surface proteins and implications for anaplasmosis serodiagnosis and vaccine development. Anim Health Res Rev 2005, 6(1):75-89. 10.1079/AHR2005104, 16164010.
21. Brayton KA, Kappmeyer LS, Herndon DR, Dark MJ, Tibbals DL, Palmer GH, McGuire TC, Knowles DP. Complete genome sequencing of Anaplasma marginale reveals that the surface is skewed to two superfamilies of outer membrane proteins. Proc Natl Acad Sci USA 2005, 102(3):844-849. 10.1073/pnas.0406656102, 545514, 15618402.
22. de la Fuente J, Kocan KM, Almazan C, Blouin EF. Targeting the tick-pathogen interface for novel control strategies. Front Biosci 2008, 13:6947-6956. 10.2741/3201, 18508707.
23. Bishop R, Lambson B, Wells C, Pandit P, Osaso J, Nkonge C, Morzaria S, Musoke A, Nene V. A cement protein of the tick Rhipicephalus appendiculatus, located in the secretory e cell granules of the type III salivary gland acini, induces strong antibody responses in cattle. Int J Parasitol 2002, 32(7):833-842. 10.1016/S0020-7519(02)00027-9, 12062554.
24. Paesen GC, Adams PL, Harlos K, Nuttall PA, Stuart DI. Tick histamine-binding proteins: isolation, cloning, and three-dimensional structure. Mol Cell 1999, 3(5):661-671. 10.1016/S1097-2765(00)80359-7, 10360182.
25. Labuda M, Trimnell AR, Lickova M, Kazimirova M, Davies GM, Lissina O, Hails RS, Nuttall PA. An antivector vaccine protects against a lethal vector-borne pathogen. PLoS Pathog 2006, 2(4):e27. 10.1371/journal.ppat.0020027, 1424664,1424664, 16604154.
26. Hayashi CY, Lewis RV. Molecular architecture and evolution of a modular spider silk protein gene. Science 2000, 287(5457):1477-1479. 10.1126/science.287.5457.1477, 10688794.
27. Alarcon-Chaidez FJ, Sun J, Wikel SK. Transcriptome analysis of the salivary glands of Dermacentor andersoni Stiles (Acari: Ixodidae). Insect Biochem Mol Biol 2007, 37(1):48-71. 10.1016/j.ibmb.2006.10.002, 17175446.
28. Santos IK, Valenzuela JG, Ribeiro JM, de Castro M, Costa JN, Costa AM, da Silva ER, Neto OB, Rocha C, Daffre S, et al. Gene discovery in Boophilus microplus, the cattle tick: the transcriptomes of ovaries, salivary glands, and hemocytes. Ann N Y Acad Sci 2004, 1026:242-246. 10.1196/annals.1307.037, 15604500.
29. Mulenga A, Blandon M, Khumthong R. The molecular basis of the Amblyomma americanum tick attachment phase. Exp Appl Acarol 2007, 41(4):267-287. 10.1007/s10493-007-9064-3, 17406795.
30. Donohue KV, Khalil SM, Mitchell RD, Sonenshine DE, Roe RM. Molecular characterization of the major hemelipoglycoprotein in ixodid ticks. Insect Mol Biol 2008, 17(3):197-208. 10.1111/j.1365-2583.2008.00794.x, 18477238.
31. Almazan C, Kocan KM, Bergman DK, Garcia-Garcia JC, Blouin EF, de la Fuente J. Identification of protective antigens for the control of Ixodes scapularis infestations using cDNA expression library immunization. Vaccine 2003, 21(13-14):1492-1501. 10.1016/S0264-410X(02)00683-7, 12615446.
32. de la Fuente J, Almazan C, Blas-Machado U, Naranjo V, Mangold AJ, Blouin EF, Gortazar C, Kocan KM. The tick protective antigen, 4D8, is a conserved protein involved in modulation of tick blood ingestion and reproduction. Vaccine 2006, 24(19):4082-4095. 10.1016/j.vaccine.2006.02.046, 16580098.
33. Almazan C, Blas-Machado U, Kocan KM, Yoshioka JH, Blouin EF, Mangold AJ, de la Fuente J. Characterization of three Ixodes scapularis cDNAs protective against tick infestations. Vaccine 2005, 23(35):4403-4416. 10.1016/j.vaccine.2005.04.012, 16005748.
34. Almazan C, Kocan KM, Blouin EF, de la Fuente J. Vaccination with recombinant tick antigens for the control of Ixodes scapularis adult infestations. Vaccine 2005, 23(46-47):5294-5298. 10.1016/j.vaccine.2005.08.004, 16153760.
35. de la Fuente J, Almazan C, Naranjo V, Blouin EF, Meyer JM, Kocan KM. Autocidal control of ticks by silencing of a single gene by RNA interference. Biochem Biophys Res Commun 2006, 344(1):332-338. 10.1016/j.bbrc.2006.03.109, 16630571.
36. Nijhof AM, Taoufik A, de la Fuente J, Kocan KM, de Vries E, Jongejan F. Gene silencing of the tick protective antigens, Bm86, Bm91 and subolesin, in the one-host tick Boophilus microplus by RNA interference. Int J Parasitol 2007, 37(6):653-662. 10.1016/j.ijpara.2006.11.005, 1885961, 17196597.
37. Kocan KM, Manzano-Roman R, de la Fuente J. Transovarial silencing of the subolesin gene in three-host ixodid tick species after injection of replete females with subolesin dsRNA. Parasitol Res 2007, 100(6):1411-1415. 10.1007/s00436-007-0483-1, 17372765.
38. de la Fuente J, Maritz-Olivier C, Naranjo V, Ayoubi P, Nijhof AM, Almazan C, Canales M, Perez de la Lastra JM, Galindo RC, Blouin EF, et al. Evidence of the role of tick subolesin in gene expression. BMC Genomics 2008, 9(1):372. 10.1186/1471-2164-9-372, 2518936, 18673577.
39. Galindo RC, Doncel-Perez E, Zivkovic Z, Naranjo V, Gortazar C, Mangold AJ, Martin-Hernando MP, Kocan KM, de la Fuente J. Tick subolesin is an ortholog of the akirins described in insects and vertebrates. Dev Comp Immunol 2009, 33(4):612-617. 10.1016/j.dci.2008.11.002, 19041667.
40. de la Fuente J, Blouin EF, Manzano-Roman R, Naranjo V, Almazan C, Perez de la Lastra JM, Zivkovic Z, Massung RF, Jongejan F, Kocan KM. Differential expression of the tick protective antigen subolesin in anaplasma marginale- and A. phagocytophilum-infected host cells. Ann N Y Acad Sci 2008, 1149:27-35. 10.1196/annals.1428.056, 19120168.
41. Borghesi LA, Lynes MA. Stress proteins as agents of immunological change: some lessons from metallothionein. Cell Stress Chaperones 1996, 1(2):99-108. 10.1379/1466-1268(1996)001<0099:SPAAOI>2.3.CO;2, 248461, 9222595.
42. Dallinger R. Metallothionein research in terrestrial invertebrates: synopsis and perspectives. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1996, 113(2):125-133. 10.1016/0742-8413(95)02078-0, 8646613.
43. Dutsch-Wicherek M, Sikora J, Tomaszewska R. The possible biological role of metallothionein in apoptosis. Front Biosci 2008, 13:4029-4038. 10.2741/2991, 18508497.
44. Mannick EE, Schurr JR, Zapata A, Lentz JJ, Gastanaduy M, Cote RL, Delgado A, Correa P, Correa H. Gene expression in gastric biopsies from patients infected with Helicobacter pylori. Scand J Gastroenterol 2004, 39(12):1192-1200. 10.1080/00365520410003588, 15742995.
45. Wiese L, Kurtzhals JA, Penkowa M. Neuronal apoptosis, metallothionein expression and proinflammatory responses during cerebral malaria in mice. Exp Neurol 2006, 200(1):216-226.
46. Baerwald MR, Welsh AB, Hedrick RP, May B. Discovery of genes implicated in whirling disease infection and resistance in rainbow trout using genome-wide expression profiling. BMC Genomics 2008, 9:37. 10.1186/1471-2164-9-37, 2257940, 18218127.
47. Hirano T, Murakami M, Fukada T, Nishida K, Yamasaki S, Suzuki T. Roles of zinc and zinc signaling in immunity: zinc as an intracellular signaling molecule. Adv Immunol 2008, 97:149-176. full_text, 18501770.
48. Uzarowska A, Dionisio G, Sarholz B, Piepho HP, Xu M, Ingvardsen CR, Wenzel G, Lubberstedt T. Validation of candidate genes putatively associated with resistance to SCMV and MDMV in maize (Zea mays L.) by expression profiling. BMC Plant Biol 2009, 9:15. 10.1186/1471-2229-9-15, 2669481, 19187556.
49. Saldivar L, Guerrero FD, Miller RJ, Bendele KG, Gondro C, Brayton KA. Microarray analysis of acaricide-inducible gene expression in the southern cattle tick, Rhipicephalus (Boophilus) microplus. Insect Mol Biol 2008, 17(6):597-606. 10.1111/j.1365-2583.2008.00831.x, 18834453.
50. Kurtti TJ, Munderloh UG, Ahlstrand GG, Johnson RC. Borrelia burgdorferi in tick cell culture: growth and cellular adherence. J Med Entomol 1988, 25(4):256-261.
51. Munderloh UG, Jauron SD, Fingerle V, Leitritz L, Hayes SF, Hautman JM, Nelson CM, Huberty BW, Kurtti TJ, Ahlstrand GG, et al. Invasion and intracellular development of the human granulocytic ehrlichiosis agent in tick cell culture. J Clin Microbiol 1999, 37(8):2518-2524. 85271, 10405394.
52. Ribeiro MF, Passos LM, Guimaraes AM. Ultrastructure of Anaplasma marginale with an inclusion appendage, isolated in Minas Gerais State, Brazil. Vet Parasitol 1997, 70(4):271-277. 10.1016/S0304-4017(97)00004-6, 9211652.
53. de la Fuente J, Garcia-Garcia JC, Blouin EF, McEwen BR, Clawson D, Kocan KM. Major surface protein 1a effects tick infection and transmission of Anaplasma marginale. Int J Parasitol 2001, 31(14):1705-1714. 10.1016/S0020-7519(01)00287-9, 11730800.
54. Munderloh UG, Blouin EF, Kocan KM, Ge NL, Edwards WL, Kurtti TJ. Establishment of the tick (Acari:Ixodidae)-borne cattle pathogen Anaplasma marginale (Rickettsiales:Anaplasmataceae) in tick cell culture. J Med Entomol 1996, 33(4):656-664.
55. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215(3):403-410.
56. Schefe JH, Lehmann KE, Buschmann IR, Unger T, Funke-Kaiser H. Quantitative real-time RT-PCR data analysis: current concepts and the novel "gene expression's CT difference" formula. J Mol Med 2006, 84(11):901-910. 10.1007/s00109-006-0097-6, 16972087.