Immunohistochemical characterization of the chemosensory pulmonary neuroepithelial bodies in the naked mole-rat reveals a unique adaptive phenotype

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Pan, Jie ^a,b   Park, Thomas J ^c   Cutz, Ernest ^a,b,d   Yeger, Herman ^a,b,d  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE; CELL PROTEIN; CYCLINE; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE 1 ALPHA; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE 2 ALPHA; PEPTIDE; SEROTONIN; SYNAPTIC VESCLE PROTEIN 2; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR MASH1; UNCLASSIFIED DRUG; UVOMORULIN; BIOLOGICAL MARKER; CARBON DIOXIDE; OXYGEN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE EXPRESSION; HETEROCEPHALUS; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; NEUROEPITHELIAL BODY; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PULMONARY NEUROEPITHELIAL BODY; RAT; SPECIES COMPARISON; SPECIES DIFFERENCE; WISTAR RAT; ADAPTATION; ANIMAL; CELL ADHESION; CYTOLOGY; GENE EXPRESSION REGULATION; INNERVATION; LUNG; METABOLISM; MOLE RAT; NERVOUS SYSTEM DEVELOPMENT; NEUROSECRETION; PHENOTYPE; PHYSIOLOGY;

HETEROCEPHALUS GLABER; MAMMALIA; RATTUS NORVEGICUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOMARKERS; CARBON DIOXIDE; CELL ADHESION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; LUNG; MOLE RATS; NEUROEPITHELIAL BODIES; NEUROGENESIS; NEUROSECRETORY SYSTEMS; OXYGEN; PHENOTYPE;

EID: 84918822217     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112623     Document Type: Article

References (32)

1. Buffenstein R (2005) The naked mole-rat: a new long-living model for human aging research. J Gerontol A Biol Sci Med Sci 60: 1369-1377.
2. Buffenstein R (2008) Negligible senescence in the longest living rodent, the naked mole-rat: insights from a successfully aging species. J Comp Physiol B 178: 439-445.
3. Rodriguez KA, Wywial E, Perez VI, Lambert AJ, Edrey YH, et al. (2011) Walking the oxidative stress tightrope: a perspective from the naked mole-rat, the longest-lived rodent. Curr Pharm Des 17: 2290-2307.
4. Tian X, Azpurua J, Hine C, Vaidya A, Myakishev-Rempel M, et al. (2013) High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat. Nature 499: 346-349.
5. Azpurua J, Seluanov A (2013) Long-lived cancer-resistant rodents as a new model species for cancer research. Front Genet 3: 319.
6. Gladyshev VN, Zhang G, Wang J (2011) The naked mole rat genome: understanding aging through genome analysis. Aging 3: 1124.
7. Smith ES, Omerbasic D, Lechner SG, Anirudhan G, Lapatsina L, et al. (2011) The molecular basis of acid insensitivity in the African naked mole-rat. Science 334: 1557-1560.
8. LaVinka PC, Park TJ (2012) Blunted behavioral and c-Fos responses to acidic fumes in the African naked mole-rat. PLoS One 7:e45060.
9. 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 PhysiolA Neuroethol Sens Neural Behav Physiol 195: 419-427.
10. Nathaniel TI, Saras A, Umesiri FE, Olajuyigbe F (2009) Tolerance to oxygen deprivation in the hippocampal slices of naked mole rats. J Integr Neurosci 8: 123-136.
11. Larson J, Park TJ (2009) Extreme hypoxia tolerance of naked mole-rat brain. Neuroreport 20: 1634-1637.
12. Peterson BL, Larson J, Buffenstein R, Park TJ, Fall CP (2012) Blunted neuronal calcium response to hypoxia in naked mole-rat hippocampus. PLoS One 7:e31568.
13. Peterson BL, Park TJ, Larson J (2012) Adult naked mole-rat brain retains the NMDA receptor subunit GluN2D associated with hypoxia tolerance in neonatal animals. Neurosci Lett 506: 342-345.
14. Edrey YH, Medina DX, Gaczynska M, Osmulski PA, Oddo S, et al. (2013) Amyloid beta and the longest-lived rodent: the naked mole-rat as a model for natural protection from Alzheimer's disease. Neurobiol Aging 34: 2352-2360.
15. Maina JN, Gebreegziabher Y, Woodley R, Buffenstein R (2001) Effects of change in environmental temperature and natural shifts in carbon dioxide and oxygen concentrations on the lungs of captive naked mole-rats (Heterocephalus glaber): a morphological and morphometric study. J Zool (Lond) 253: 371-382.
16. Cutz E, Pan J, Yeger H (2009) The role of NOX2 and "novel oxidases" in airway chemoreceptor O(2) signaling. Adv Exp Med Biol 648: 427-438.
17. Cutz E, Pan J, Yeger H, Domnik NJ, Fisher JT (2013) Recent advances and controversies on the role of pulmonary neuroepithelial bodies as airway sensors. Semin Cell Dev Biol 24: 40-50.
18. Park TJ, Lu Y, Juttner R, Smith ES, Hu J, et al. (2008) Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). PLoS Biol 6:e13.
19. Pan J, Luk C, Kent G, Cutz E, Yeger H (2006) Pulmonary neuroendocrine cells, airway innervation and smooth muscle are altered in Cftr null mice. Am J Respir Cell Mol Biol 35: 320-326.
20. Penuela S, Gehi R, Laird DW (2013) The biochemistry and function of pannexin channels. Biochim Biophys Acta 1821: 15-22.
21. Wong AP, Keating A, Waddell TK (2009) Airway regeneration: the role of the Clara cell secretory protein and the cells that express it. Cytotherapy 11: 676-687.
22. Yeger H, Pan J, Cutz E (2009) Precursors and stem cells of the pulmonary neuroendocrine system in developing mammalian lung. In: Zaccone G, et al, editors. Airway Chemoreceptors in the Vertebrates. 306: 287-306.
23. Brouns I, Oztay F, Pintelon I, De Proost I, Lembrechts R, et al. (2009) Neurochemical pattern of the complex innervation of neuroepithelial bodies in mouse lungs. Histochem Cell Biol 131: 55-74.
24. Brouns I, DeProost I, Pintelon I, Timmermans JP, Adriaensen D (2006) Sensory receptors in the airways: neurochemical coding of smooth muscle-associated airway receptors and pulmonary neuroepithelial body innervation. Auton Neurosci 126-127: 307-319.
25. Miki M, Ball DW, Linnoila RI (2012) Insights into the achaete-scute homolog-1 gene (hASH1) in normal and neoplastic human lung. Lung Cancer 75: 58-65.
26. McGovern S, Pan J, Oliver G, Cutz E, Yeger H (2010) The role of hypoxia and neurogenic genes (Mash-1 and Prox-1) in the developmental programming and maturation of pulmonary neuroendocrine cells in fetal mouse lung. Lab Invest 90: 180-195.
27. Semenza GL (2012) Hypoxia inducible factors in physiology and medicine. Cell 148: 399-408.
28. Patel SA, Simon MC (2008) Biology of hypoxia-inducible factor 22alpha in development and disease. Cell Death Differ 15: 628-634.
29. Lewis KN, Andziak B, Yang T, Buffenstein R (2013) The naked mole-rat response to oxidative stress:just deal with it. Antioxid Redox Signal 19: 1388-1399.
30. Pan J, Yeger H, Ratcliffe P, Bishop T, Cutz E (2012) Hyperplasia of pulmonary neuroepithelial bodies (NEB) in lungs of prolyl-hydoxylase-1 (PHD-1) deficient mice. Adv Exp Med Biol 758: 149-155.
31. Gu X, Karp PH, Brody SL, Pierce RA, Welsh MJ, et al. (2014) Volatile-sensing functions for pulmonary neuroendocrine cells. Am J Respir Cell Mol Biol 50: 637-646.
32. Burnstock G, Brouns I, Adriaensen D, Timmermans JP (2012) Purinergic signaling in the airways. Pharmacol Rev 64: 834-868.