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PMID: 28002412 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Piezo2 senses airway stretch and mediates lung inflation-induced apnoea.

Nature ·Vol. 541 ·No. 7636 ·2017-00-12 ·Pages 176-181

Nonomura K, Woo SH, Chang RB, Gillich A, Qiu Z, Francisco AG, Ranade SS, Liberles SD, Patapoutian A

Abstract

Respiratory dysfunction is a notorious cause of perinatal mortality in infants and sleep apnoea in adults, but the mechanisms of respiratory control are not clearly understood. Mechanical signals transduced by airway-innervating sensory neurons control respiration; however, the physiological significance and molecular mechanisms of these signals remain obscured. Here we show that global and sensory neuron-specific ablation of the mechanically activated ion channel Piezo2 causes respiratory distress and death in newborn mice. Optogenetic activation of Piezo2+ vagal sensory neurons causes apnoea in adult mice. Moreover, induced ablation of Piezo2 in sensory neurons of adult mice causes decreased neuronal responses to lung inflation, an impaired Hering-Breuer mechanoreflex, and increased tidal volume under normal conditions. These phenotypes are reproduced in mice lacking Piezo2 in the nodose ganglion. Our data suggest that Piezo2 is an airway stretch sensor and that Piezo2-mediated mechanotransduction within various airway-innervating sensory neurons is critical for establishing efficient respiration at birth and maintaining normal breathing in adults.

MeSH Terms
Animals Animals, Newborn Apnea/genetics,physiopathology Death Female Ion Channels/deficiency,genetics,metabolism Lung/physiology,physiopathology Male Mechanotransduction, Cellular/genetics,physiology Mice Nodose Ganglion/metabolism Reflex/genetics,physiology Respiration Sensory Receptor Cells/metabolism Tidal Volume
Chemicals
Ion Channels Piezo2 protein, mouse
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Nonomura Keiko
Howard Hughes Medical Institute, Molecular and Cellular Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, California 92037, USA.
Woo Seung-Hyun
Howard Hughes Medical Institute, Molecular and Cellular Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, California 92037, USA.
Chang Rui B
Department of Cell Biology, Harvard Medical School, Boston, Massachusetts 02115, USA.
Gillich Astrid
Howard Hughes Medical Institute, Department of Biochemistry, Stanford University School of Medicine, Stanford, California 94305, USA.
Qiu Zhaozhu
Howard Hughes Medical Institute, Molecular and Cellular Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, California 92037, USA. | Genomics Institute of the Novartis Research Foundation, San Diego, California 92121, USA.
Francisco Allain G
Howard Hughes Medical Institute, Molecular and Cellular Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, California 92037, USA.
Ranade Sanjeev S
Howard Hughes Medical Institute, Molecular and Cellular Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, California 92037, USA.
Liberles Stephen D
Department of Cell Biology, Harvard Medical School, Boston, Massachusetts 02115, USA.
Patapoutian Ardem
Howard Hughes Medical Institute, Molecular and Cellular Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, California 92037, USA.
References (56)
56 references, click to expand
  1. The branching programme of mouse lung development.
    Nature. 2008 Jun 5;453(7196):745-50 PMID: 18463632
  2. Mechanical stretch-induced serotonin release from pulmonary neuroendocrine cells: implications for lung development.
    Am J Physiol Lung Cell Mol Physiol. 2006 Jan;290(1):L185-93 PMID: 16100287
  3. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels.
    Science. 2010 Oct 1;330(6000):55-60 PMID: 20813920
  4. Hering-Breuer reflex in normal adults and in patients with chronic obstructive pulmonary disease and interstitial fibrosis.
    Respiration. 2001;68(2):140-4 PMID: 11287827
  5. Physiological and pathophysiological implications of upper airway reflexes in humans.
    Jpn J Physiol. 2000 Feb;50(1):3-14 PMID: 10866692
  6. The Role of PIEZO2 in Human Mechanosensation.
    N Engl J Med. 2016 Oct 6;375(14 ):1355-1364 PMID: 27653382
  7. Ion channel and receptor mechanisms of bladder afferent nerve sensitivity.
    Auton Neurosci. 2010 Feb 16;153(1-2):26-32 PMID: 19632906
  8. Thyroid hormone receptor repression is linked to type I pneumocyte-associated respiratory distress syndrome.
    Nat Med. 2011 Oct 16;17 (11):1466-72 PMID: 22001906
  9. Pulmonary vagal innervation is required to establish adequate alveolar ventilation in the newborn lamb.
    J Appl Physiol (1985). 1998 Sep;85(3):849-59 PMID: 9729557
  10. Influence of volume dependency and timing of airway occlusions on the Hering-Breuer reflex in infants.
    J Appl Physiol (1985). 1998 Dec;85(6):2033-9 PMID: 9843523
  11. Structural and functional architecture of respiratory networks in the mammalian brainstem.
    Philos Trans R Soc Lond B Biol Sci. 2009 Sep 12;364(1529):2577-87 PMID: 19651658
  12. Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow.
    J Exp Med. 2001 Mar 19;193(6):741-54 PMID: 11257140
  13. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase.
    Curr Biol. 1998 Dec 3;8(24):1323-6 PMID: 9843687
  14. Ventilatory response to hyperoxia in newborn mice heterozygous for the transcription factor Phox2b.
    Am J Physiol Regul Integr Comp Physiol. 2006 Jun;290(6):R1691-6 PMID: 16410396
  15. Vagal Sensory Neuron Subtypes that Differentially Control Breathing.
    Cell. 2015 Apr 23;161(3):622-33 PMID: 25892222
  16. Neurotrophin-4 deficient mice have a loss of vagal intraganglionic mechanoreceptors from the small intestine and a disruption of short-term satiety.
    J Neurosci. 2001 Nov 1;21(21):8602-15 PMID: 11606648
  17. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography.
    Am J Respir Crit Care Med. 1997 Sep;156(3 Pt 1):766-75 PMID: 9309991
  18. A family of distal arthrogryposis type 5 due to a novel PIEZO2 mutation.
    Am J Med Genet A. 2015 May;167A(5):1100-6 PMID: 25712306
  19. Pulmonary sensory and reflex responses in the mouse.
    J Appl Physiol (1985). 2006 Sep;101(3):986-92 PMID: 16675617
  20. Piezo2 is the principal mechanotransduction channel for proprioception.
    Nat Neurosci. 2015 Dec;18(12):1756-62 PMID: 26551544
  21. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis.
    Development. 2000 Apr;127(8):1671-9 PMID: 10725243
  22. Recent advances and contraversies on the role of pulmonary neuroepithelial bodies as airway sensors.
    Semin Cell Dev Biol. 2013 Jan;24(1):40-50 PMID: 23022441
  23. Hypoglossal neuropathology and respiratory activity in pompe mice.
    Front Physiol. 2011 Jun 30;2:31 PMID: 21747768
  24. Substance P expression in TRPV1 and trkA-positive dorsal root ganglion neurons innervating the mouse lung.
    Respir Physiol Neurobiol. 2004 Nov 30;144(1):15-24 PMID: 15522699
  25. Leptin receptor expression in hindbrain Glp-1 neurons regulates food intake and energy balance in mice.
    J Clin Invest. 2011 Jun;121(6):2413-21 PMID: 21606595
  26. Gain-of-function mutations in the mechanically activated ion channel PIEZO2 cause a subtype of Distal Arthrogryposis.
    Proc Natl Acad Sci U S A. 2013 Mar 19;110(12):4667-72 PMID: 23487782
  27. The role of respiratory control disorders in SIDS.
    Respir Physiol Neurobiol. 2005 Nov 15;149(1-3):343-53 PMID: 16122993
  28. Phenotypic distinctions between neural crest and placodal derived vagal C-fibres in mouse lungs.
    J Physiol. 2010 Dec 1;588(Pt 23):4769-83 PMID: 20937710
  29. Bronchopulmonary afferent nerves.
    Respirology. 2003 Sep;8(3):291-301 PMID: 14528878
  30. KCa1.1 channel contributes to cell excitability in unmyelinated but not myelinated rat vagal afferents.
    Am J Physiol Cell Physiol. 2011 Jun;300(6):C1393-403 PMID: 21325638
  31. Significance of vagal innervation in perinatal breathing and gas exchange.
    Respir Physiol. 2000 Feb;119(2-3):133-41 PMID: 10722856
  32. Interpreting neonatal lethal phenotypes in mouse mutants: insights into gene function and human diseases.
    Physiol Rev. 2009 Jan;89(1):1-26 PMID: 19126753
  33. PIEZO2 is required for mechanotransduction in human stem cell-derived touch receptors.
    Nat Neurosci. 2015 Jan;18(1):10-6 PMID: 25469543
  34. Computer assisted recognition and quantitation of the effects of airborne chemicals acting at different areas of the respiratory tract in mice.
    Arch Toxicol. 1994;68(8):490-9 PMID: 7802589
  35. Piezo2 is the major transducer of mechanical forces for touch sensation in mice.
    Nature. 2014 Dec 4;516(7529):121-5 PMID: 25471886
  36. Breath-holding and its breakpoint.
    Exp Physiol. 2006 Jan;91(1):1-15 PMID: 16272264
  37. Overview of the innervation of the lung.
    Curr Opin Pharmacol. 2002 Jun;2(3):211-5 PMID: 12020459
  38. Localisation of P2Y1 and P2Y4 receptors in dorsal root, nodose and trigeminal ganglia of the rat.
    Histochem Cell Biol. 2003 Nov;120(5):415-26 PMID: 14564529
  39. Biallelic Loss of Proprioception-Related PIEZO2 Causes Muscular Atrophy with Perinatal Respiratory Distress, Arthrogryposis, and Scoliosis.
    Am J Hum Genet. 2016 Nov 3;99(5):1206-1216 PMID: 27843126
  40. The ion channel ASIC2 is required for baroreceptor and autonomic control of the circulation.
    Neuron. 2009 Dec 24;64(6):885-97 PMID: 20064394
  41. Nodose ganglia-modulatory effects on respiration.
    Physiol Res. 2013;62(3):227-35 PMID: 23489183
  42. Effect of gas composition on liquid secretion by explants of distal lung of fetal rat in submersion culture.
    Am J Physiol. 1993 Nov;265(5 Pt 1):L512-7 PMID: 8238540
  43. The Role of the Paratrigeminal Nucleus in Vagal Afferent Evoked Respiratory Reflexes: A Neuroanatomical and Functional Study in Guinea Pigs.
    Front Physiol. 2015 Dec 21;6:378 PMID: 26733874
  44. Effect of central hypervolemia on respiratory function.
    J Physiol Pharmacol. 2007 Nov;58 Suppl 5(Pt 1):9-15 PMID: 18204110
  45. Neurones in a discrete region of the nucleus tractus solitarius are required for the Breuer-Hering reflex in rat.
    J Physiol. 1990 Aug;427:261-80 PMID: 2213599
  46. Isoflurane abolishes spontaneous firing of serotonin neurons and masks their pH/CO₂ chemosensitivity.
    J Neurophysiol. 2015 Apr 1;113(7):2879-88 PMID: 25695656
  47. Sensory nerves in lung and airways.
    Compr Physiol. 2014 Jan;4(1):287-324 PMID: 24692141
  48. Piezo2 is required for Merkel-cell mechanotransduction.
    Nature. 2014 May 29;509(7502):622-6 PMID: 24717433
  49. Functional organization of the parabrachial complex and intertrigeminal region in the control of breathing.
    Respir Physiol Neurobiol. 2004 Nov 15;143(2-3):115-25 PMID: 15519549
  50. Merkel cells and neurons keep in touch.
    Trends Cell Biol. 2015 Feb;25(2):74-81 PMID: 25480024
  51. An overview of the anatomy and physiology of slowly adapting pulmonary stretch receptors.
    Respir Physiol. 2001 Mar;125(1-2):17-31 PMID: 11240150
  52. Inflammatory signals enhance piezo2-mediated mechanosensitive currents.
    Cell Rep. 2012 Sep 27;2(3):511-7 PMID: 22921401
  53. Mechanically Activated Ion Channels.
    Neuron. 2015 Sep 23;87(6):1162-79 PMID: 26402601
  54. Central and peripheral factors contributing to obstructive sleep apneas.
    Respir Physiol Neurobiol. 2013 Nov 1;189(2):344-53 PMID: 23770311
  55. Evidence for multiple sensory circuits in the brain arising from the respiratory system: an anterograde viral tract tracing study in rodents.
    Brain Struct Funct. 2015 Nov;220(6):3683-99 PMID: 25158901
  56. Voltage-gated sodium channels in nociceptive versus non-nociceptive nodose vagal sensory neurons innervating guinea pig lungs.
    J Physiol. 2008 Mar 1;586(5):1321-36 PMID: 18187475
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2017-00-12
Epub
2016-00-21
Pages
176-181
Language
English
Region
England
NLM ID
0410462
PMCID
PMC5267560
Subset
IM
Grants
NCCIH NIH HHS · DP1 AT009497 · United States
NIDCR NIH HHS · R01 DE022358 · United States
NHLBI NIH HHS · R01 HL132255 · United States
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