Ticks, Ixodes scapularis, Feed Repeatedly on White-Footed Mice despite Strong Inflammatory Response: An Expanding Paradigm for Understanding Tick–Host Interactions
Ticks transmit infectious agents including bacteria, viruses and protozoa. However, their transmission may be compromised by host resistance to repeated tick feeding. Increasing host resistance to repeated tick bites is well known in laboratory animals, including intense inflammation at the bite sit...
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doaj-794597d9e61a44a3bf320ba7df540eca2020-11-24T23:57:49ZengFrontiers Media S.A.Frontiers in Immunology1664-32242017-12-01810.3389/fimmu.2017.01784306013Ticks, Ixodes scapularis, Feed Repeatedly on White-Footed Mice despite Strong Inflammatory Response: An Expanding Paradigm for Understanding Tick–Host InteractionsJennifer M. Anderson0Ian N. Moore1Bianca M. Nagata2José M. C. Ribeiro3Jesus G. Valenzuela4Daniel E. Sonenshine5Daniel E. Sonenshine6Vector Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases (NIH), Rockville, MD, United StatesInfectious Disease and Pathogenesis Section, Comparative Medicine Branch, National Institute of Allergy and Infectious Diseases (NIH), Rockville, MD, United StatesInfectious Disease and Pathogenesis Section, Comparative Medicine Branch, National Institute of Allergy and Infectious Diseases (NIH), Rockville, MD, United StatesVector Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases (NIH), Rockville, MD, United StatesVector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases (NIH), Rockville, MD, United StatesVector Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases (NIH), Rockville, MD, United StatesDepartment of Biological Sciences, Old Dominion University, Norfolk, VA, United StatesTicks transmit infectious agents including bacteria, viruses and protozoa. However, their transmission may be compromised by host resistance to repeated tick feeding. Increasing host resistance to repeated tick bites is well known in laboratory animals, including intense inflammation at the bite sites. However, it is not known whether this also occurs in wild rodents such as white-footed mice, Peromyscus leucopus, and other wildlife, or if it occurs at all. According to the “host immune incompetence” hypothesis, if these mice do not have a strong inflammatory response, they would not reject repeated tick bites by Ixodes scapularis. To test this hypothesis, histopathological studies were done comparing dermal inflammation in P. leucopus versus guinea pigs, Cavia porcellus, repeatedly infested with I. scapularis. In P. leucopus, the immune cell composition was like that seen in laboratory mouse models, with some differences. However, there was a broad sessile lesion with intact dermal architecture, likely enabling the ticks to continue feeding unimpeded. In contrast, in C. porcellus, there was a relatively similar mixed cellular profile, but there also was a large, leukocyte-filled cavitary lesion and scab-like hyperkeratotic changes to the epidermal layer, along with itching and apparent pain. Ticks attached to sensitized C. porcellus fed poorly or were dislodged, presumably due to the weakened anchoring of the tick’s mouthparts cemented in the heavily inflamed and disintegrating dermal tissues. This is the first time that the architecture of the skin lesions has been recognized as a major factor in understanding tick–host tolerance versus tick bite rejection. These findings broadly strengthen previous work done on lab animal models but also help explain why I. scapularis can repeatedly parasitize white-footed mice, supporting the “immune evasion theory” but cannot repeatedly parasitize other, non-permissive hosts such as guinea pigs.http://journal.frontiersin.org/article/10.3389/fimmu.2017.01784/fullIxodes scapularisPeromyscus leucopusinflammationT-cellsmacrophagessessile |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Jennifer M. Anderson Ian N. Moore Bianca M. Nagata José M. C. Ribeiro Jesus G. Valenzuela Daniel E. Sonenshine Daniel E. Sonenshine |
spellingShingle |
Jennifer M. Anderson Ian N. Moore Bianca M. Nagata José M. C. Ribeiro Jesus G. Valenzuela Daniel E. Sonenshine Daniel E. Sonenshine Ticks, Ixodes scapularis, Feed Repeatedly on White-Footed Mice despite Strong Inflammatory Response: An Expanding Paradigm for Understanding Tick–Host Interactions Frontiers in Immunology Ixodes scapularis Peromyscus leucopus inflammation T-cells macrophages sessile |
author_facet |
Jennifer M. Anderson Ian N. Moore Bianca M. Nagata José M. C. Ribeiro Jesus G. Valenzuela Daniel E. Sonenshine Daniel E. Sonenshine |
author_sort |
Jennifer M. Anderson |
title |
Ticks, Ixodes scapularis, Feed Repeatedly on White-Footed Mice despite Strong Inflammatory Response: An Expanding Paradigm for Understanding Tick–Host Interactions |
title_short |
Ticks, Ixodes scapularis, Feed Repeatedly on White-Footed Mice despite Strong Inflammatory Response: An Expanding Paradigm for Understanding Tick–Host Interactions |
title_full |
Ticks, Ixodes scapularis, Feed Repeatedly on White-Footed Mice despite Strong Inflammatory Response: An Expanding Paradigm for Understanding Tick–Host Interactions |
title_fullStr |
Ticks, Ixodes scapularis, Feed Repeatedly on White-Footed Mice despite Strong Inflammatory Response: An Expanding Paradigm for Understanding Tick–Host Interactions |
title_full_unstemmed |
Ticks, Ixodes scapularis, Feed Repeatedly on White-Footed Mice despite Strong Inflammatory Response: An Expanding Paradigm for Understanding Tick–Host Interactions |
title_sort |
ticks, ixodes scapularis, feed repeatedly on white-footed mice despite strong inflammatory response: an expanding paradigm for understanding tick–host interactions |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Immunology |
issn |
1664-3224 |
publishDate |
2017-12-01 |
description |
Ticks transmit infectious agents including bacteria, viruses and protozoa. However, their transmission may be compromised by host resistance to repeated tick feeding. Increasing host resistance to repeated tick bites is well known in laboratory animals, including intense inflammation at the bite sites. However, it is not known whether this also occurs in wild rodents such as white-footed mice, Peromyscus leucopus, and other wildlife, or if it occurs at all. According to the “host immune incompetence” hypothesis, if these mice do not have a strong inflammatory response, they would not reject repeated tick bites by Ixodes scapularis. To test this hypothesis, histopathological studies were done comparing dermal inflammation in P. leucopus versus guinea pigs, Cavia porcellus, repeatedly infested with I. scapularis. In P. leucopus, the immune cell composition was like that seen in laboratory mouse models, with some differences. However, there was a broad sessile lesion with intact dermal architecture, likely enabling the ticks to continue feeding unimpeded. In contrast, in C. porcellus, there was a relatively similar mixed cellular profile, but there also was a large, leukocyte-filled cavitary lesion and scab-like hyperkeratotic changes to the epidermal layer, along with itching and apparent pain. Ticks attached to sensitized C. porcellus fed poorly or were dislodged, presumably due to the weakened anchoring of the tick’s mouthparts cemented in the heavily inflamed and disintegrating dermal tissues. This is the first time that the architecture of the skin lesions has been recognized as a major factor in understanding tick–host tolerance versus tick bite rejection. These findings broadly strengthen previous work done on lab animal models but also help explain why I. scapularis can repeatedly parasitize white-footed mice, supporting the “immune evasion theory” but cannot repeatedly parasitize other, non-permissive hosts such as guinea pigs. |
topic |
Ixodes scapularis Peromyscus leucopus inflammation T-cells macrophages sessile |
url |
http://journal.frontiersin.org/article/10.3389/fimmu.2017.01784/full |
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