Blunted Behavioral and C Fos Responses to Acidic Fumes in the African Naked Mole-Rat

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  LaVinka, Pamela Colleen ^a,b   Park, Thomas J ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; PROTEIN C FOS;

ACIDOSIS; AIRBORNE PARTICLE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; AVERSION; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; FUME; HUMIDITY; INFORMATION PROCESSING; MOLE RAT; MOUSE; NEUROIMAGING; NONHUMAN; RAT; SENSORY NERVE; SIGNAL TRANSDUCTION; SOLITARY TRACT NUCLEUS; TRIGEMINAL NUCLEUS;

ACETIC ACID; AFRICA; AMMONIA; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CELL COUNT; IRRITANTS; MICE; MICE, INBRED C57BL; MOLE RATS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; SOLITARY NUCLEUS; STAINING AND LABELING; TRIGEMINAL NUCLEI;

HETEROCEPHALUS GLABER; RODENTIA; VERTEBRATA;

EID: 84866445425     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045060     Document Type: Article

References (55)

1. Ernstgård L, Iregren A, Sjögren B, Johanson G, (2006) Acute effects of exposure to vapours of acetic acid in humans. Toxicol Lett. 165(1): 22-30.
2. Wang YY, Chang RB, Allgood SD, Silver WL, Liman ER, (2011) A TRPA1-dependent mechanism for the pungent sensation of weak acids. J Gen Physiol. 137(6): 493-505.
3. Park TJ, Lu Y, Jüttner R, Smith ES, Hu J, et al. (2008) Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). PLoS Biol. 6(1): e13.
4. Smith ES, Omerbašić D, Lechner SG, Anirudhan G, Lapatsina L, et al. (2011) The molecular basis of acid insensitivity in the African naked mole-rat. Science. 334(6062): 1557-60.
5. Bennett NC Faulkes CG (2000) African Mole-Rats: Ecology and Eusociality. Cambridge: University Press, 29-52p.
6. Jarvis JUM, (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212: 571-573.
7. Brett RA (1991) The population structure of naked mole-rat colonies. In: Sherman PW, Jarvis JUM, Alexander RD, editors. The biology of the naked mole rat. Princeton (New Jersey): Princeton University Press. 97-136.
8. Sharabi K, Lecuona E, Helenius IT, Beitel GJ, Sznajder JI, et al. (2009) Sensing, physiological effects and molecular response to elevated CO2 levels in eukaryotes. J Cell Mol Med. 13(11-12): 4304-18.
9. Wang YY, Chang RB, Liman ER, (2010) TRPA1 is a component of the nociceptive response to CO2. J Neurosci. 30(39): 12958-63.
10. Leffler A, Mönter B, Koltzenburg M, (2006) The role of the capsaicin receptor TRPV1 and acid-sensing ion channels (ASICS) in proton sensitivity of subpopulations of primary nociceptive neurons in rats and mice. Neuroscience. 139(2): 699-709.
11. Sekizawa SI, Tsubone H, (1994) Nasal receptors responding to noxious chemical iirritants. Respir Physiol 96: 37-48.
12. LaVinka PC, Brand A, Landau VJ, Wirtshafter D, Park TJ, (2009) Extreme tolerance to ammonia fumes in African naked mole-rats: animals that naturally lack neuropeptides from trigeminal chemosensory nerve fibers. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 195(5): 419-27.
13. McCulloch PF, Panneton WM, (1997) Fos immunohistochemical determination of brainstem neuronal activation in the muskrat after nasal stimulation. Neuroscience. 78(3): 913-25.
14. Anton F, Herdegen T, Peppel P, Leah JD, (1991) c-FOS-like immunoreactivity in rat brainstem neurons following noxious chemical stimulation of the nasal mucosa. Neuroscience. 41(2-3): 629-41.
15. Takeda M, Tanimoto T, Ikeda M, Nishikawa T, Kawanishi N, et al. (1999) Changes in c-Fos expression induced by noxious stimulation in the trigeminal spinal nucleus caudalis and C1 spinal neurons of rats after hyperbaric exposure. Arch Histol Cytol. 62(2): 165-70.
16. Baraniuk JN, Kim D, (2007) Nasal reflexes, the nasal cycle, and sneeze. Curr Allergy Asthma Rep. 7(2): 105-11.
17. Geppetti P, Fusco BM, Alessandri M, Tramontana M, Maggi CA, et al. (1991) Kallidin applied to the human nasal mucosa produces algesic response not blocked by capsaicin desensitization. Regul Pept. 17 33(3): 321-9.
18. Kaise T, Akamatsu Y, Ohmori K, Ishii A, Karasawa A, (2001) Inhibitory effect of olopatadine hydrochloride on the sneezing response induced by intranasal capsaicin challenge in guinea pigs. Jpn J Pharmacol. 86(2): 258-61.
19. Niel L and Weary DM (2007) Rats avoid exposure to carbon dioxide and argon. Applied Animal Behaviour Science, 107; 100-109.
20. Artwohl J, Hill T, Comer C, Park T, (2002) Naked mole-rats: unique opportunities and husbandry challenges. Lab Anim (NY). 31(5): 32-6.
21. Paxinos G and Watson C (2005) The Rat Brain in Stereotaxic Coordinates, Fifth edition. Academic Press, San Diego.
22. Paxinos G and Franklin KBJ (2004) The Mouse Brain in Stereotaxic Coordinates, Second Edition, Academic Press, San Diego.
23. Xiao J, Levitt JB, Buffenstein R, (2006) A stereotaxic atlas of the brain of the naked mole-rat (Heterocephalus glaber). Neuroscience. 141(3): 1415-35.
24. Alheid GF, Jiao W, McCrimmon DR, (2011) Caudal nuclei of the rat nucleus of the solitary tract differentially innervate respiratory compartments within the ventrolateral medulla. Neuroscience. 190: 207-27.
25. Cruz Jde C, Bonagamba LG, Stern JE, Machado BH, (2010) Fos expression in the NTS in response to peripheral chemoreflex activation in awake rats. Auton Neurosci. 152(1 2): 27-34.
26. Takakura AC, Moreira TS, Colombari E, West GH, Stornetta RL, et al. (2006) Peripheral chemoreceptor inputs to retrotrapezoid nucleus (RTN) CO2-sensitive neurons in rats. J Physiol. 15;572(Pt 2): 503-23.
27. Bryant BP, (2005) Mechanisms of Somatosensory Neuronal Sensitivity to Alkaline pH. Chem Senses (30) Suppl 1():: i196-i197.
28. Carstens E, Kuenzler N, Handwerker HO, (1998) Activation of neurons in rat trigeminal subnucleus caudalis by different irritant chemicals applied to oral or ocular mucosa. J Neurophysiol (802) (): 465-92.
29. Anton F, Peppel P, (1991) Central projections of trigeminal primary afferents innervating the nasal mucosa: a horseradish peroxidase study in the rat. Neuroscience. 41(2-3): 617-28.
30. Lipski J, Ezure K, Wong She RB, (1991) Identification of neurons receiving input from pulmonary rapidly adapting receptors in the cat. J Physiol. 443: 55-77.
31. Corson J, Aldridge A, Wilmoth K, Erisir A, (2012) A survey of oral cavity afferents to the rat nucleus tractus solitarii. J of Comp Neurol. 520 (3): 495-527.
32. Burn CC, Peters A, Day MJ, Mason GJ, (2006) Long-term effects of cage-cleaning frequency and bedding type on laboratory rat health, welfare, and handleability: a cross-laboratory study. Lab Anim. 40(4): 353-70.
33. Silverman J, Bays DW, Baker SP, (2009) Ammonia and carbon dioxide concentrations in disposable and reusable static mouse cages. Lab Anim (NY). 38(1): 16-23.
34. O'Connor TP, Lee A, Jarvis JU, Buffenstein R, (2002) Prolonged longevity in naked mole-rats: age-related changes in metabolism, body composition and gastrointestinal function. Comp Biochem Physiol A Comp Physiol 133: 835-842.
35. Johansen K, Lykkeboe G, Weber RE, and Maloiy GM (1976) Blood respiratory properties in the naked mole rat Heterocephalus glaber, a mammal of low body temperature. Respir. Physiol, 28, 303-314.
36. Larson J, Park TJ, (2009) Extreme hypoxia tolerance of naked mole-rat brain. Neuroreport. 20(18): 1634-7.
37. Peterson BL, Larson J, Buffenstein R, Park TJ, Fall CP, (2012a) Blunted neuronal calcium response to hypoxia in naked mole-rat hippocampus. PLoS One. 2012 7(2): e31568.
38. Peterson BL, Park TJ, Larson J, (2012b) Adult naked mole-rat brain retains the NMDA receptor subunit GluN2D associated with hypoxia tolerance in neonatal mammals. Neurosci Lett. 506(2): 342-5.
39. Park TJ, Comer C, Carol A, Lu Y, Hong HS, et al. (2003) Somatosensory organization and behavior in naked mole-rats: II. Peripheral structures, innervation, and selective lack of neuropeptides associated with thermoregulation and pain. J Comp Neurol. 465(1): 104 20.
40. Anton F, Euchner I, Handwerker HO, (1992) Psychophysical examination of pain induced by defined CO2 pulses applied to the nasal mucosa. Pain 49: 53-60.
41. Chen X, Gallar J, Pozo MA, Baeza M, Belmonte C, (1995) CO2 stimulation of the cornea: a comparison between human sensation and nerve activity in polymodal nociceptive afferents of the cat. Eur J Neurosci. 7(6): 1154-63.
42. Lundblad L, Lundberg JM, Brodin E, Anggard A, (1983) Origin and distribution of capsaicin-sensitive substance P-immunoreactive nerves in the nasal mucosa. Acta Otolaryngol 96(5-6): 485-493.
43. Taylor-Clark TE, Kollarik M, MacGlashan DW Jr, Undem BJ, (2005) Nasal sensory nerve populations responding to histamine and capsaicin. J Allergy Clin Immunol 116(6): 1282-1288.
44. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, et al. (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 21(3): 531-43.
45. Fujita F, Uchida K, Moriyama T, Shima A, Shibasaki K, et al. (2008) Intracellular alkalization causes pain sensation through activation of TRPA1 in mice. J Clin Invest. 118(12): 4049-57.
46. Dhaka A, Uzzell V, Dubin AE, Mathur J, Petrus M, et al. (2009) TRPV1 is activated by both acidic and basic pH. J Neurosci. 29(1): 153-8.
47. Arai T, Ohkuri T, Yasumatsu K, Kaga T, Ninomiya Y, (2010) The role of transient receptor potential vanilloid-1 on neural responses to acids by the chorda tympani, glossopharyngeal and superior laryngeal nerves in mice. Neuroscience 165(4): 1476-89.
48. Holzer P, (2009) Acid-sensitive ion channels and receptors. Handbook of experimental pharmacology 194: 283-332.
49. Kim EB, Fang X, Fushan AA, Huang Z, Lobanov AV, et al. (2011) Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Nature. 12;479(7372): 223 7.
50. Brand A, Smith ES, Lewin GR, Park TJ, (2010) Functional neurokinin and NMDA receptor activity in an animal naturally lacking substance P: the naked mole-rat. PLoS One. 21 5(12): e15162.
51. Smith ES, Blass GR, Lewin GR, Park TJ, (2010) Absence of histamine-induced itch in the African naked mole-rat and "rescue" by Substance P. Mol Pain. 6: 29.
52. Liu L, Pugh W, Ma H, Simon SA, (1993) Identification of acetylcholine receptors in adult rat trigeminal ganglion neurons. Brain Res 617: 37-42.
53. Alimohammadi H, Silver WL, (2000) Evidence for nicotinic acetylcholine receptors on nasal trigeminal nerve endings of the rat. Chem Senses. 25(1): 61-6.
54. Miura M, Okada J, Takayama K, Suzuki T, (1994) Neuronal expression of Fos and Jun protein in the rat medulla and spinal cord after anoxic and hypercapnic stimulations. Neurosci Lett. 178(2): 227-30.
55. Takada SH, Sampaio CA, Allemandi W, Ito PH, Takase LF, et al. (2011) A modified rat model of neonatal anoxia: Development and evaluation by pulseoximetry, arterial gasometry and Fos immunoreactivity. J Neurosci Methods. 198(1): 62-9.