Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber).
In all mammals, tissue inflammation leads to pain and behavioral sensitization to thermal and mechanical stimuli called hyperalgesia. We studied pain mechanisms in the African naked mole-rat, an unusual rodent species that lacks pain-related neuropeptides (e.g., substance P) in cutaneous sensory fib...
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2008
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oai:doaj.org-article:73915162b7a54fe0be6856fd5a5b44ab2021-11-25T05:33:32ZSelective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber).1544-91731545-788510.1371/journal.pbio.0060013https://doaj.org/article/73915162b7a54fe0be6856fd5a5b44ab2008-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18232734/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885In all mammals, tissue inflammation leads to pain and behavioral sensitization to thermal and mechanical stimuli called hyperalgesia. We studied pain mechanisms in the African naked mole-rat, an unusual rodent species that lacks pain-related neuropeptides (e.g., substance P) in cutaneous sensory fibers. Naked mole-rats show a unique and remarkable lack of pain-related behaviors to two potent algogens, acid and capsaicin. Furthermore, when exposed to inflammatory insults or known mediators, naked mole-rats do not display thermal hyperalgesia. In contrast, naked mole-rats do display nocifensive behaviors in the formalin test and show mechanical hyperalgesia after inflammation. Using electrophysiology, we showed that primary afferent nociceptors in naked mole-rats are insensitive to acid stimuli, consistent with the animal's lack of acid-induced behavior. Acid transduction by sensory neurons is observed in birds, amphibians, and fish, which suggests that this tranduction mechanism has been selectively disabled in the naked mole-rat in the course of its evolution. In contrast, nociceptors do respond vigorously to capsaicin, and we also show that sensory neurons express a transient receptor potential vanilloid channel-1 ion channel that is capsaicin sensitive. Nevertheless, the activation of capsaicin-sensitive sensory neurons in naked mole-rats does not produce pain-related behavior. We show that capsaicin-sensitive nociceptors in the naked mole-rat are functionally connected to superficial dorsal horn neurons as in mice. However, the same nociceptors are also functionally connected to deep dorsal horn neurons, a connectivity that is rare in mice. The pain biology of the naked mole-rat is unique among mammals, thus the study of pain mechanisms in this unusual species can provide major insights into what constitutes "normal" mammalian nociception.Thomas J ParkYing LuRené JüttnerEwan St J SmithJing HuAntje BrandChristiane WetzelNevena MilenkovicBettina ErdmannPaul A HeppenstallCharles E LauritoSteven P WilsonGary R LewinPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 6, Iss 1, p e13 (2008) |
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Biology (General) QH301-705.5 |
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Biology (General) QH301-705.5 Thomas J Park Ying Lu René Jüttner Ewan St J Smith Jing Hu Antje Brand Christiane Wetzel Nevena Milenkovic Bettina Erdmann Paul A Heppenstall Charles E Laurito Steven P Wilson Gary R Lewin Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). |
| description |
In all mammals, tissue inflammation leads to pain and behavioral sensitization to thermal and mechanical stimuli called hyperalgesia. We studied pain mechanisms in the African naked mole-rat, an unusual rodent species that lacks pain-related neuropeptides (e.g., substance P) in cutaneous sensory fibers. Naked mole-rats show a unique and remarkable lack of pain-related behaviors to two potent algogens, acid and capsaicin. Furthermore, when exposed to inflammatory insults or known mediators, naked mole-rats do not display thermal hyperalgesia. In contrast, naked mole-rats do display nocifensive behaviors in the formalin test and show mechanical hyperalgesia after inflammation. Using electrophysiology, we showed that primary afferent nociceptors in naked mole-rats are insensitive to acid stimuli, consistent with the animal's lack of acid-induced behavior. Acid transduction by sensory neurons is observed in birds, amphibians, and fish, which suggests that this tranduction mechanism has been selectively disabled in the naked mole-rat in the course of its evolution. In contrast, nociceptors do respond vigorously to capsaicin, and we also show that sensory neurons express a transient receptor potential vanilloid channel-1 ion channel that is capsaicin sensitive. Nevertheless, the activation of capsaicin-sensitive sensory neurons in naked mole-rats does not produce pain-related behavior. We show that capsaicin-sensitive nociceptors in the naked mole-rat are functionally connected to superficial dorsal horn neurons as in mice. However, the same nociceptors are also functionally connected to deep dorsal horn neurons, a connectivity that is rare in mice. The pain biology of the naked mole-rat is unique among mammals, thus the study of pain mechanisms in this unusual species can provide major insights into what constitutes "normal" mammalian nociception. |
| format |
article |
| author |
Thomas J Park Ying Lu René Jüttner Ewan St J Smith Jing Hu Antje Brand Christiane Wetzel Nevena Milenkovic Bettina Erdmann Paul A Heppenstall Charles E Laurito Steven P Wilson Gary R Lewin |
| author_facet |
Thomas J Park Ying Lu René Jüttner Ewan St J Smith Jing Hu Antje Brand Christiane Wetzel Nevena Milenkovic Bettina Erdmann Paul A Heppenstall Charles E Laurito Steven P Wilson Gary R Lewin |
| author_sort |
Thomas J Park |
| title |
Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). |
| title_short |
Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). |
| title_full |
Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). |
| title_fullStr |
Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). |
| title_full_unstemmed |
Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). |
| title_sort |
selective inflammatory pain insensitivity in the african naked mole-rat (heterocephalus glaber). |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2008 |
| url |
https://doaj.org/article/73915162b7a54fe0be6856fd5a5b44ab |
| work_keys_str_mv |
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