Tick Immune System: What Is Known, the Interconnections, the Gaps, and the Challenges.

Publisher: Frontiers Research Foundation] Country of Publication: Switzerland NLM ID: 101560960 Publication Model: eCollection Cited Medium: Internet ISSN: 1664-3224 (Electronic) Linking ISSN: 16643224 NLM ISO Abbreviation: Front Immunol Subsets: MEDLINE

Original Publication: [Lausanne : Frontiers Research Foundation]

Immunity, Cellular* ; Immunity, Humoral*; Saliva/*immunology ; Salivary Glands/*immunology ; Tick-Borne Diseases/*immunology ; Ticks/*immunology; Animals ; Host-Parasite Interactions ; Humans ; Saliva/metabolism ; Salivary Glands/metabolism ; Tick-Borne Diseases/metabolism ; Tick-Borne Diseases/transmission ; Ticks/metabolism

Ticks are ectoparasitic arthropods that necessarily feed on the blood of their vertebrate hosts. The success of blood acquisition depends on the pharmacological properties of tick saliva, which is injected into the host during tick feeding. Saliva is also used as a vehicle by several types of pathogens to be transmitted to the host, making ticks versatile vectors of several diseases for humans and other animals. When a tick feeds on an infected host, the pathogen reaches the gut of the tick and must migrate to its salivary glands via hemolymph to be successfully transmitted to a subsequent host during the next stage of feeding. In addition, some pathogens can colonize the ovaries of the tick and be transovarially transmitted to progeny. The tick immune system, as well as the immune system of other invertebrates, is more rudimentary than the immune system of vertebrates, presenting only innate immune responses. Although simpler, the large number of tick species evidences the efficiency of their immune system. The factors of their immune system act in each tick organ that interacts with pathogens; therefore, these factors are potential targets for the development of new strategies for the control of ticks and tick-borne diseases. The objective of this review is to present the prevailing knowledge on the tick immune system and to discuss the challenges of studying tick immunity, especially regarding the gaps and interconnections. To this end, we use a comparative approach of the tick immune system with the immune system of other invertebrates, focusing on various components of humoral and cellular immunity, such as signaling pathways, antimicrobial peptides, redox metabolism, complement-like molecules and regulated cell death. In addition, the role of tick microbiota in vector competence is also discussed.
Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
(Copyright © 2021 Fogaça, Sousa, Pavanelo, Esteves, Martins, Urbanová, Kopáček and Daffre.)

Virus Evol. 2016 Oct 26;2(2):vew033. (PMID: 28058113)
J Biol Chem. 2009 Dec 11;284(50):34735-46. (PMID: 19828445)
Nat Microbiol. 2016 Mar 14;1:16023. (PMID: 27572642)
Immunol Rev. 2004 Apr;198:116-26. (PMID: 15199959)
Peptides. 2006 Apr;27(4):667-74. (PMID: 16191451)
Dev Comp Immunol. 2014 Jan;42(1):25-35. (PMID: 23721820)
Histochem Cell Biol. 2002 May;117(5):431-40. (PMID: 12029490)
Dev Comp Immunol. 2018 Feb;79:86-94. (PMID: 29061482)
Immunol Rev. 2004 Apr;198:169-84. (PMID: 15199962)
Front Physiol. 2017 Sep 06;8:608. (PMID: 28932198)
Immunol Rev. 2011 Mar;240(1):129-40. (PMID: 21349091)
Adv Exp Med Biol. 2010;708:137-62. (PMID: 21528697)
Ticks Tick Borne Dis. 2018 Jul;9(5):1364-1371. (PMID: 29886187)
PLoS One. 2013 Apr 10;8(4):e61187. (PMID: 23593426)
Dev Comp Immunol. 2014 Jan;42(1):42-6. (PMID: 23545286)
Front Cell Infect Microbiol. 2018 May 29;8:176. (PMID: 29896452)
J Med Entomol. 2001 Jul;38(4):514-9. (PMID: 11476331)
PLoS Negl Trop Dis. 2015 May 13;9(5):e0003754. (PMID: 25970599)
Biopolymers. 2007;88(3):413-26. (PMID: 17245752)
J Immunol. 2015 Dec 15;195(12):5696-706. (PMID: 26546607)
PLoS Pathog. 2017 Sep 27;13(9):e1006645. (PMID: 28953952)
Annu Rev Immunol. 2007;25:697-743. (PMID: 17201680)
Nat Commun. 2017 Aug 4;8(1):184. (PMID: 28775250)
PLoS One. 2019 Apr 3;14(4):e0214794. (PMID: 30943246)
Curr Opin Immunol. 2003 Feb;15(1):12-9. (PMID: 12495727)
Apoptosis. 2009 Aug;14(8):950-60. (PMID: 19495985)
J Innate Immun. 2013;5(5):444-55. (PMID: 23689401)
Mol Cell Biol. 2006 Nov;26(21):7821-31. (PMID: 16894030)
J Biol Chem. 2007 Jan 19;282(3):2056-68. (PMID: 17068333)
Insect Biochem Mol Biol. 2000 Mar;30(3):195-205. (PMID: 10732987)
PLoS Negl Trop Dis. 2018 Apr 13;12(4):e0006410. (PMID: 29652888)
Sci Adv. 2017 Aug 16;3(8):e1700585. (PMID: 28835919)
Nat Commun. 2016 Feb 09;7:10507. (PMID: 26856261)
Front Cell Infect Microbiol. 2017 Jun 22;7:281. (PMID: 28690983)
PLoS One. 2012;7(6):e38544. (PMID: 22685581)
Annu Rev Cell Dev Biol. 1996;12:393-416. (PMID: 8970732)
Front Cell Infect Microbiol. 2014 Aug 22;4:116. (PMID: 25202684)
PLoS One. 2012;7(1):e30861. (PMID: 22292064)
J Med Entomol. 2008 Nov;45(6):1156-9. (PMID: 19058642)
Science. 2010 Mar 26;327(5973):1644-8. (PMID: 20223948)
J Mol Biol. 1993 Jul 20;232(2):327-33. (PMID: 8345514)
Dev Comp Immunol. 2017 Sep;74:32-39. (PMID: 28408334)
Cell Host Microbe. 2014 Jan 15;15(1):58-71. (PMID: 24439898)
Nat Rev Microbiol. 2004 Oct;2(10):820-32. (PMID: 15378046)
Front Microbiol. 2017 Feb 14;8:223. (PMID: 28261180)
PLoS Pathog. 2011 Mar;7(3):e1001320. (PMID: 21445237)
Dev Comp Immunol. 2014 Jan;42(1):3-15. (PMID: 24012863)
Parasit Vectors. 2017 Feb 23;10(1):103. (PMID: 28231846)
ISME J. 2016 Aug;10(8):1846-55. (PMID: 26882265)
Front Cell Infect Microbiol. 2017 Apr 28;7:129. (PMID: 28503490)
Nature. 1981 Jul 16;292(5820):246-8. (PMID: 7019715)
PLoS Negl Trop Dis. 2014 Apr 24;8(4):e2823. (PMID: 24762775)
Dev Comp Immunol. 2014 Oct;46(2):439-47. (PMID: 24924263)
PLoS Negl Trop Dis. 2015 Apr 23;9(4):e0003689. (PMID: 25905888)
Toxicol Pathol. 2007 Jun;35(4):495-516. (PMID: 17562483)
BMC Genomics. 2020 Feb 10;21(1):137. (PMID: 32041526)
Sci Rep. 2019 Sep 11;9(1):13110. (PMID: 31511580)
Insect Biochem Mol Biol. 2007 May;37(5):399-408. (PMID: 17456435)
Front Cell Infect Microbiol. 2017 Mar 16;7:73. (PMID: 28361038)
Front Biosci. 2008 May 01;13:6938-46. (PMID: 18508706)
J Biochem Mol Biol. 2005 Mar 31;38(2):128-50. (PMID: 15826490)
Nature. 2015 Feb 5;518(7537):98-101. (PMID: 25470067)
Apoptosis. 2006 Sep;11(9):1643-51. (PMID: 16820968)
Pathogens. 2020 Apr 22;9(4):. (PMID: 32331444)
Science. 1999 May 21;284(5418):1313-8. (PMID: 10334979)
Parasit Vectors. 2017 Dec 19;10(1):613. (PMID: 29258559)
J Med Entomol. 2002 Mar;39(2):376-83. (PMID: 11931039)
Future Microbiol. 2011 Mar;6(3):265-77. (PMID: 21449839)
EMBO Rep. 2005 Oct;6(10):979-84. (PMID: 16170305)
Nat Rev Microbiol. 2020 Oct;18(10):587-600. (PMID: 32651470)
Trends Parasitol. 2012 Oct;28(10):437-46. (PMID: 22902521)
Insect Biochem Mol Biol. 2013 Feb;43(2):146-52. (PMID: 23202267)
Trends Parasitol. 2018 Dec;34(12):1017-1026. (PMID: 30343986)
Science. 2005 Nov 4;310(5749):847-50. (PMID: 16272120)
Dev Comp Immunol. 2014 Jan;42(1):85-92. (PMID: 23684730)
Cell Host Microbe. 2016 Jul 13;20(1):91-8. (PMID: 27374407)
Nat Immunol. 2005 Sep;6(9):946-53. (PMID: 16086017)
Cell Host Microbe. 2008 Jun 12;3(6):364-74. (PMID: 18541213)
Parasit Vectors. 2018 Mar 2;11(1):121. (PMID: 29499735)
Parasit Vectors. 2020 Dec 1;13(1):603. (PMID: 33261663)
J Infect Dis. 2013 Dec 1;208(11):1830-40. (PMID: 23901084)
Dev Comp Immunol. 2014 Jan;42(1):16-24. (PMID: 23632253)
Ticks Tick Borne Dis. 2020 May;11(3):101402. (PMID: 32035896)
Insects. 2018 Dec 14;9(4):. (PMID: 30558130)
Curr Opin Insect Sci. 2014 Sep 1;3:14-21. (PMID: 25309850)
Front Physiol. 2019 May 29;10:654. (PMID: 31191351)
Front Biosci. 2008 May 01;13:7046-63. (PMID: 18508715)
J Cell Sci. 2012 Dec 15;125(Pt 24):5944-9. (PMID: 23038775)
Trends Parasitol. 2016 Mar;32(3):207-218. (PMID: 26776329)
Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10086-91. (PMID: 10468566)
Infect Immun. 2008 Nov;76(11):5429-35. (PMID: 18779339)
Dev Comp Immunol. 2009 Aug;33(8):913-9. (PMID: 19454333)
Insect Biochem Mol Biol. 2006 Apr;36(4):291-9. (PMID: 16551543)
Trends Immunol. 2001 Jan;22(1):47-52. (PMID: 11286692)
J Clin Invest. 2009 Dec;119(12):3652-65. (PMID: 19920352)
Front Immunol. 2017 May 09;8:539. (PMID: 28536580)
J Proteomics. 2015 Oct 14;128:58-68. (PMID: 26189360)
PLoS One. 2012;7(5):e36783. (PMID: 22611464)
J Biol Chem. 1999 Sep 3;274(36):25330-4. (PMID: 10464258)
Exp Appl Acarol. 2017 Dec;73(3-4):401-428. (PMID: 29181673)
Mol Ecol. 2017 Jun;26(11):2905-2921. (PMID: 28281305)
Int J Parasitol. 2017 Aug;47(9):569-583. (PMID: 28577881)
Nat Commun. 2017 Feb 14;8:14401. (PMID: 28195158)
Eur J Biochem. 1993 Apr 1;213(1):591-7. (PMID: 8097463)
Ticks Tick Borne Dis. 2019 Oct;10(6):101252. (PMID: 31255534)
Parasit Vectors. 2017 Feb 15;10(1):81. (PMID: 28202075)
Immunity. 2009 Apr 17;30(4):588-98. (PMID: 19362021)
J Biol Chem. 2003 Dec 5;278(49):48928-34. (PMID: 14519762)
Autophagy. 2018;14(2):233-242. (PMID: 29130360)
J Cell Biol. 2011 Dec 12;195(6):931-42. (PMID: 22123830)
PLoS One. 2015 Jul 16;10(7):e0133240. (PMID: 26181517)
Dev Comp Immunol. 2004 Mar;28(3):191-200. (PMID: 14642886)
Proc Biol Sci. 2019 Feb 27;286(1897):20182207. (PMID: 30963836)
Thromb Res. 1992 Oct 1;68(1):1-32. (PMID: 1448796)
Proc Natl Acad Sci U S A. 2012 Nov 13;109(46):18915-20. (PMID: 23027947)
Front Cell Infect Microbiol. 2017 Dec 08;7:509. (PMID: 29276701)
Parasitol Res. 2002 Aug;88(8):781-4. (PMID: 12122439)
Dev Comp Immunol. 2016 Jun;59:1-14. (PMID: 26724380)
Exp Appl Acarol. 2005;35(4):317-33. (PMID: 15969464)
Front Physiol. 2019 May 03;10:529. (PMID: 31130872)
Insect Mol Biol. 2014 Aug;23(4):457-65. (PMID: 24779891)
Nat Immunol. 2008 Aug;9(8):908-16. (PMID: 18604211)
Res Immunol. 1990 Nov-Dec;141(9):908-10. (PMID: 2129210)
Parasitology. 2004;129 Suppl:S67-81. (PMID: 15938505)
Parasit Vectors. 2015 Dec 10;8:632. (PMID: 26653035)
J Innate Immun. 2011;3(6):623-30. (PMID: 21811049)
Proc Natl Acad Sci U S A. 2017 Jan 31;114(5):E781-E790. (PMID: 28096373)
Dev Comp Immunol. 2015 Jan;48(1):55-64. (PMID: 25224405)
Ticks Tick Borne Dis. 2018 Sep;9(6):1421-1430. (PMID: 30207274)
Rev Bras Parasitol Vet. 2014 Apr-Jun;23(2):150-6. (PMID: 25054492)
PLoS Biol. 2007 Sep;5(9):e238. (PMID: 17803358)
Proc Natl Acad Sci U S A. 2019 Jan 2;116(1):205-210. (PMID: 30559180)
PLoS Biol. 2006 Jan;4(1):e4. (PMID: 16336044)
Parasitol Res. 2011 Nov;109(5):1341-9. (PMID: 21537978)
Insect Biochem Mol Biol. 2003 Aug;33(8):841-51. (PMID: 12878230)
Immunity. 2012 Apr 20;36(4):658-67. (PMID: 22464169)
Dev Comp Immunol. 2015 May;50(1):58-67. (PMID: 25530095)
Dev Comp Immunol. 2009 Apr;33(4):489-98. (PMID: 18948134)
Insect Biochem Mol Biol. 2005 Sep;35(9):991-1004. (PMID: 15979000)
Curr Opin Virol. 2019 Aug;37:26-36. (PMID: 31176069)
Front Cell Infect Microbiol. 2020 May 08;10:211. (PMID: 32457850)
Nature. 2011 Aug 24;476(7361):454-7. (PMID: 21866160)
Annu Rev Microbiol. 1987;41:103-26. (PMID: 3318666)
Infect Immun. 2013 Jul;81(7):2415-25. (PMID: 23630955)
Nucleic Acids Res. 2014 Aug;42(14):9436-46. (PMID: 25053841)
Cell Host Microbe. 2007 Jul 12;2(1):7-18. (PMID: 18005713)
Exp Appl Acarol. 2005;36(3):207-23. (PMID: 16132735)
Int Immunol. 2006 Dec;18(12):1671-80. (PMID: 17035349)
Sci Rep. 2019 Jun 24;9(1):9073. (PMID: 31235752)
Science. 2012 Feb 17;335(6070):856-9. (PMID: 22282475)
J Invertebr Pathol. 2020 Nov;177:107481. (PMID: 33035534)
PLoS Pathog. 2010 Apr 01;6(4):e1000833. (PMID: 20368968)
Parasit Vectors. 2010 Jul 27;3:63. (PMID: 20663211)
Infect Immun. 2011 Jan;79(1):321-9. (PMID: 20956566)
Cell. 2020 Sep 3;182(5):1328-1340.e13. (PMID: 32814014)
Immunobiology. 2006;211(4):213-36. (PMID: 16697916)
J Biol Chem. 2000 Sep 22;275(38):29264-7. (PMID: 10880508)
Acta Biochim Pol. 2005;52(3):633-8. (PMID: 16175238)
J Biol Chem. 1983 Dec 10;258(23):14485-9. (PMID: 6643497)
J Biol Chem. 2014 May 2;289(18):12813-22. (PMID: 24662290)
Mol Biol Evol. 2015 Aug;32(8):2111-29. (PMID: 25908671)
Int J Genomics. 2017;2017:7636513. (PMID: 28265565)
FASEB J. 2013 Dec;27(12):4745-56. (PMID: 23964076)
Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14715-20. (PMID: 20679214)
Front Cell Infect Microbiol. 2013 Jul 16;3:26. (PMID: 23875177)
Infect Immun. 2019 May 21;87(6):. (PMID: 30910791)
J Med Entomol. 2003 Jan;40(1):78-81. (PMID: 12597657)
BMC Microbiol. 2011 Jan 06;11(1):6. (PMID: 21211038)
PLoS One. 2018 Aug 27;13(8):e0202270. (PMID: 30148833)
Parasit Vectors. 2015 Nov 18;8:599. (PMID: 26582129)
Antioxid Redox Signal. 2006 Sep-Oct;8(9-10):1865-79. (PMID: 16987039)
Exp Parasitol. 2001 Oct;99(2):66-72. (PMID: 11748959)
Sci Rep. 2017 Dec 14;7(1):17554. (PMID: 29242567)
Parasit Vectors. 2018 Jan 22;11(1):48. (PMID: 29357911)
Peptides. 2012 Sep;37(1):120-7. (PMID: 22749988)
Cell. 1996 Sep 20;86(6):973-83. (PMID: 8808632)
Open Biol. 2019 Mar 29;9(3):190009. (PMID: 30862253)
FASEB J. 2004 Sep;18(12):1447-9. (PMID: 15247144)
J Clin Invest. 1985 Oct;76(4):1436-9. (PMID: 4056036)
PLoS Genet. 2015 Mar 27;11(3):e1005120. (PMID: 25815810)
Front Cell Infect Microbiol. 2016 Feb 10;6:20. (PMID: 26904518)
J Insect Physiol. 2013 Feb;59(2):138-47. (PMID: 22960307)
Nat Microbiol. 2017 Mar 01;2:17020. (PMID: 28248301)
BMC Microbiol. 2011 Feb 28;11:45. (PMID: 21356105)
J Biol Chem. 2008 Feb 8;283(6):3217-3223. (PMID: 18065421)
FEMS Microbiol Rev. 2018 May 1;42(3):233-258. (PMID: 29893904)
Acta Trop. 2018 Jul;183:43-56. (PMID: 29625092)
Nature. 2011 Aug 24;476(7361):450-3. (PMID: 21866159)
Mol Cell Biol. 2007 Jun;27(12):4578-88. (PMID: 17438142)
Parasitol Today. 1989 Jun;5(6):171-6. (PMID: 15463205)
Biochim Biophys Acta. 2002 Sep 19;1572(2-3):414-21. (PMID: 12223283)
Insect Biochem Mol Biol. 2005 Jul;35(7):677-89. (PMID: 15894185)
Nat Commun. 2020 May 5;11(1):2205. (PMID: 32371874)
J Invertebr Pathol. 2006 Oct;93(2):96-104. (PMID: 16793056)
PLoS Negl Trop Dis. 2019 May 20;13(5):e0007443. (PMID: 31107912)
Eur J Biochem. 1999 Jun;262(3):680-7. (PMID: 10411628)
Front Cell Infect Microbiol. 2017 Sep 05;7:390. (PMID: 28929088)
PLoS Pathog. 2012 Jan;8(1):e1002470. (PMID: 22241995)
Cells. 2013 Mar 14;2(1):163-87. (PMID: 24709650)
Exp Appl Acarol. 1990 Oct;9(3-4):279-87. (PMID: 2261820)
J Mol Biol. 2008 Mar 28;377(3):902-13. (PMID: 18279891)
J Parasitol. 1997 Oct;83(5):815-8. (PMID: 9379283)
J Med Entomol. 2015 Nov;52(6):1193-202. (PMID: 26336264)
PLoS One. 2014 May 30;9(5):e98614. (PMID: 24878588)
Front Immunol. 2017 Jun 29;8:759. (PMID: 28706521)
Dev Comp Immunol. 2020 May;106:103606. (PMID: 31904432)
Ticks Tick Borne Dis. 2015 Sep;6(6):758-67. (PMID: 26183310)
Science. 2002 Oct 4;298(5591):159-65. (PMID: 12364793)
Cell Death Differ. 2018 Mar;25(3):486-541. (PMID: 29362479)
Front Cell Infect Microbiol. 2013 Aug 20;3:43. (PMID: 23971008)
Genes (Basel). 2012 Nov 06;3(4):702-41. (PMID: 24705082)
EMBO J. 2005 Jan 26;24(2):382-94. (PMID: 15616573)
Nat Immunol. 2010 Sep;11(9):785-97. (PMID: 20720586)
Nat Rev Microbiol. 2010 May;8(5):328-39. (PMID: 20372158)
Autophagy. 2008 Jan;4(1):79-81. (PMID: 17938584)
Cell. 2020 Dec 10;183(6):1562-1571.e12. (PMID: 33306955)
Cell Host Microbe. 2010 Jul 22;8(1):44-54. (PMID: 20638641)
Dev Comp Immunol. 2017 Mar;68:34-45. (PMID: 27871832)
J Biol Chem. 2002 Oct 18;277(42):40084-90. (PMID: 12189150)
Adv Exp Med Biol. 2010;708:122-36. (PMID: 21528696)
J Infect Dis. 2012 Oct;206(8):1233-41. (PMID: 22859824)
ISME J. 2018 Nov;12(11):2596-2607. (PMID: 29946195)
J Innate Immun. 2010;2(1):24-32. (PMID: 20375620)
EMBO J. 2005 Oct 5;24(19):3423-34. (PMID: 16163390)
FEMS Microbiol Lett. 2011 Nov;324(1):64-72. (PMID: 22092765)
Front Cell Infect Microbiol. 2017 Jun 08;7:236. (PMID: 28642842)
Viruses. 2014 Sep 23;6(9):3514-34. (PMID: 25251636)

Keywords: cell-mediated immunity; immune signaling pathway; immune system; microbiota; tick-borne pathogen

Date Created: 20210319 Date Completed: 20210915 Latest Revision: 20231111

20240829

PMC7962413

10.3389/fimmu.2021.628054

33737931