Advertisement

Sensing Environmental Factors: The Emerging Role of Receptors in Epidermal Homeostasis and Whole-Body Health

Chapter
  • 817 Downloads

Abstract

Epidermal keratinocytes have been recognized to form the water-impermeable structure and this barrier function is critical, especially for terrestrial animals. However, recent findings have dramatically changed the picture of epidermal keratinocytes, placing them at the forefront of the sensory system. Keratinocytes contains environmental sensors and a sensory information-processing system, and it generates a variety of hormones and neurotransmitters that influence whole-body states and emotions. Specifically, epidermal keratinocytes contain sensors of mechanical stress, temperature and chemical stimuli. Moreover, all the components of the hypothalamo-pituitary-adrenal (HPA) axis appear to be present in epidermal keratinocytes. These results suggest that the epidermis plays an important role in adapting whole-body physiology, and probably also emotional response, to changing environments.

Keywords

Keratinocyte Stratum corneum Neurotransmitter 

References

  1. Arima M, Shimizu Y, Sowa J, Narita T, Nishi I, Iwata N, Ozaki N, Hashimoto S, Matsunaga K (2005) Psychosomatic analysis of atopic dermatitis using a psychological test. J Dermatol 32:160–168CrossRefPubMedGoogle Scholar
  2. Ashida Y, Ogo M, Denda M (2001a) Epidermal IL-1 alpha generation is amplified at low humidities: Implications for the pathogenesis of inflammatory dermatoses. Br J Dermatol 144:238–243CrossRefPubMedGoogle Scholar
  3. Ashida Y, Denda M, Hirao T (2001b) Histamine H1 and H2 receptor antagonists accelerate skin barrier repair and prevent epidermal hyperplasia induced by barrier disruption in a dry environment. J Invest Dermatol 116:261–265CrossRefPubMedGoogle Scholar
  4. Capuron L, Miller AH (2011) Immune system to brain signaling: neuropsychopharmacological implications. Pharmacol Ther 130:226–238CrossRefPubMedPubMedCentralGoogle Scholar
  5. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824CrossRefPubMedGoogle Scholar
  6. Chung MK, Lee H, Caterina MJ (2003) Warm temperatures activate TRPV4 in mouse 308 keratinocytes. J Biol Chem 278:32037–32046CrossRefPubMedGoogle Scholar
  7. Czeisler CA, Shanahan TL, Klerman EB, Martens H, Brotman DJ, Jonathan SE, Klein T, Rizzo JF (1995) Suppression of melatonin secretion in some blind patients by exposure to bright light. N Eng J Med 332:6–11CrossRefGoogle Scholar
  8. Denda M, Denda S (2007) Air-exposed keratinocytes exhibited intracellular oscillation. Skin Res Technol 13:195–201CrossRefPubMedGoogle Scholar
  9. Denda M, Fuziwara S (2008) Visible radiation affects epidermal permeability barrier recovery: selective effects of red and blue light. J Invest Dermatol 128:1335–1336CrossRefPubMedGoogle Scholar
  10. Denda M, Nakatani M (2010) Acceleration of permeability barrier recovery by exposure of skin to 10-30 kilohertz sound. Br J Dermatol 162:503–507CrossRefPubMedGoogle Scholar
  11. Denda M, Tsutsumi M (2011) Roles of transient receptor potential proteins (TRPs) in epidermal keratinocytes transient receptor potential channels. Advan Exp Med Biol 704:847–860CrossRefGoogle Scholar
  12. Denda M, Tsutsumi M (2014) Possible role of epidermal keratinocytes in the construction of acupuncture meridians. J Acupunct Meridian Stud 7:92–94CrossRefPubMedGoogle Scholar
  13. Denda M, Sato J, Masuda Y, Tsuchiya T, Koyama J, Kuramoto M, Elias PM, Feingold KR (1998a) Exposure to a dry environment enhances epidermal permeability barrier function. J Invest Dermatol 111:858–863CrossRefGoogle Scholar
  14. Denda M, Sato J, Tsuchiya T, Elias PM, Feingold KR (1998b) Low humidity stimulates epidermal DNA synthesis and amplifies the hyperproliferative response to barrier disruption: implication for seasonal exacerbations of inflammatory dermatoses. J Invest Dermatol 111:873–878CrossRefPubMedGoogle Scholar
  15. Denda M, Fuziwara S, Inoue K, Denda S, Akamatsu H, Tomitaka A, Matsunaga K (2001) Immunoreactivity of VR1 on epidermal keratinocyte of human skin. Biochem Biophys Res Commun 285:1250–1252CrossRefPubMedGoogle Scholar
  16. Denda M, Nakatani M, Ikeyama K, Tsutsumi M, Denda S (2007a) Epidermal keratinocytes as the forefront of the sensory system. Exp Dermatol 16:157–161CrossRefPubMedGoogle Scholar
  17. Denda M, Sokabe T, Tominaga T, Tominaga M (2007b) Effects of skin surface temperature on epidermal permeability barrier homeostasis. J Invest Dermatol 127:654–659CrossRefPubMedGoogle Scholar
  18. Denda M, Tsutsumi M, Goto M, Ikeyama K, Denda S (2010a) Topical application of TRPA1 agonists and brief cold exposure accelerate skin permeability barrier recovery. J Invest Dermatol 130:1942–1945CrossRefPubMedGoogle Scholar
  19. Denda M, Tsutsumi M, Denda S (2010b) Topical application of TRPM8 agonists accelerates skin permeability barrier recovery and reduces epidermal proliferation induced by barrier insult: the role of cold-sensitive TRP receptors in epidermal permeability barrier homeostasis. Exp Dermatol 19:791–795CrossRefPubMedGoogle Scholar
  20. Denda S, Takei K, Kumamoto J, Goto M, Tsutsumi M, Denda M (2012) Oxytocin is expressed in epidermal keratinocytes and released upon stimulation with adenosine 5’-[gamma-thio]triphosphate in vitro. Exp Dermatol 21:535–537CrossRefPubMedGoogle Scholar
  21. Denda M, Takei K, Denda S (2013) How does epidermal pathology interact with mental state? Med Hypothesis 80:194–196CrossRefGoogle Scholar
  22. Dhaka A, Viswanath V, Patapoutian A (2006) TRP ion channels and temperature sensation. Ann Rev Neurosci 29:135–161CrossRefPubMedGoogle Scholar
  23. Dhaka A, Uzzell V, Dubin AE, Mathur J, Petrus M, Bandell M, Patapoutian A (2009) TRPV1 is activated by both acidic and basic pH. J Neurosci 29:153–158CrossRefPubMedPubMedCentralGoogle Scholar
  24. Ferguson JN, Young LJ, Hearn EF (2000) Social amnesia in mice lacking the oxytocin gene. Nat Genet 25:284–288CrossRefPubMedGoogle Scholar
  25. Fuziwara S, Inoue K, Denda M (2003) NMDA-type glutamate receptor is associated with cutaneous barrier homeostasis. J Invest Dermatol 120:1023–1029CrossRefPubMedGoogle Scholar
  26. Fuziwara S, Suzuki A, Inoue K, Denda M (2005) Dopamine D2-like receptor agonists accelerate barrier repair and inhibit the epidermal hyperplasia induced by barrier disruption. J Invest Dermatol 125:783–789CrossRefPubMedGoogle Scholar
  27. Gick B, Derrick D (2009) Aero-tactile integration in speech perception. Nature 462:502–504CrossRefPubMedPubMedCentralGoogle Scholar
  28. Goto M, Ikeyama K, Tsutsumi M, Denda S, Denda M (2010) Calcium ion propagation in cultured keratinocytes and other cells in skin in response to hydraulic pressure stimulation. J Cell Physiol 224:229–233PubMedGoogle Scholar
  29. Goto M, Ikeyama K, Tsutsumi M, Denda S, Denda M (2011) Phosphodiesterase inhibitors block the acceleration of skin permeability barrier repair by red light. Exp Dermatol 20:568–571CrossRefPubMedGoogle Scholar
  30. Hashiro M, Okumura M (1997) Anxiety, depression and psychosomatic symptoms in patients with atopic dermatitis: comparison with normal controls and among groups of different degrees of severity. J Dermatol Sci 14:63–67CrossRefPubMedGoogle Scholar
  31. Heffner RS (2004) Primate hearing from a mammalian perspective. Anat Rec A Discov Mol Cell Evol Biol 281:1111–1122CrossRefPubMedGoogle Scholar
  32. Hollander E, Notny S, Hanratty M (2003) Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger’s disorders. Neuropsychopharmacology 28:193–198CrossRefPubMedGoogle Scholar
  33. Hosoi J, Hariya T, Denda M, Tsuchiya T (2000) Regulation of the cutaneous allergic reaction by humidity. Contact Dermatitis 42:81–84CrossRefPubMedGoogle Scholar
  34. Huang SM, Lee H, Chung MK et al (2008) Overexpressed transient receptor potential vanilloid 3 ion channels in skin keratinocytes modulate pain sensitivity via prostaglandin E2. J Neurosci 28:13727–13737CrossRefPubMedPubMedCentralGoogle Scholar
  35. Iijima T, Witter MP, Ichikawa M, Tominaga T, Kajiwara R, Matsumoto G (1996) Entorhinal-hippocampal interactions revealed by real-time imaging. Science 72:1176–1179CrossRefGoogle Scholar
  36. Ikeyama K, Fuziwara S, Denda M (2007) Topical application of neuronal nitric oxide synthase inhibitor accelerates cutaneous barrier recovery and prevents epidermal hyperplasia induced by barrier disruption. J Invest Dermatol 127:1713–1719CrossRefPubMedGoogle Scholar
  37. Ikeyama K, Denda S, Tsutsumi M, Denda M (2010) Neuronal nitric oxide synthase in epidermis is involved in cutaneous circulatory response to mechanical stimulation. J Invest Dermatol 130:1158–1166CrossRefPubMedGoogle Scholar
  38. Ikeyama K, Nakatani M, Kumamoto J, Denda M (2013) Distinct intracellular calcium responses of individual cultured human keratinocytes to air pressure changes. Skin Res Tech 19:346–351CrossRefGoogle Scholar
  39. Inoue K, Koizumi S, Fuziwara S, Denda S, Inoue K, Denda M (2002) Functional vanilloid receptors in cultured normal human keratinocytes. Biochem Biophys Res Commun 291:124–129CrossRefPubMedGoogle Scholar
  40. Inoue K, Hosoi J, Denda M (2007) Extracellular ATP has stimulatory effects on the expression and release of IL-6 via purinergic receptors in normal human keratinocytes. J Invest Dermatol 127:362–371CrossRefPubMedGoogle Scholar
  41. Katagiri C, Sato J, Nomura J, Denda M (2003) Changes in environmental humidity affect the water-holding property of the stratum corneum and its free amino acid content, and the expression of filaggrin in the epidermis of hairless mice. J Dermatol Sci 31:29–35CrossRefPubMedGoogle Scholar
  42. Kawai N, Honda M, Nakamura S et al (2001) Catecholamines and opioid peptides increase in plasma in humans during possession trances. NeuroReport 12:3419–3423CrossRefPubMedGoogle Scholar
  43. Kirsch P, Esslinger C, Chen Q (2005) Oxytocin modulates neural circuitry for social cognition and fear in humans. J Neurosci 25:11489–11493CrossRefPubMedGoogle Scholar
  44. Liedtke W (2007) Role of TRPV ion channels in sensory transduction of osmotic stimuli in mammals. Exp Physiol 92:507–512CrossRefPubMedGoogle Scholar
  45. Miller AH, Maletic V, Raison CL (2009) Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry 65:732–741CrossRefPubMedGoogle Scholar
  46. Nakatani M, Kawasoe T, Denda M (2011) Sex difference in human fingertip recognition of micron-level randomness as unpleasant. Int J Cosmet Sci 33:346–350CrossRefPubMedGoogle Scholar
  47. Okano T, Yoshizawa T, Fukada Y (1994) Pinopsin is a chicken pineal photoreceptive molecule. Nature 372:94–97CrossRefPubMedGoogle Scholar
  48. Oohashi T, Nishina E, Honda M et al (2000) Inaudible high-frequency sounds affect brain activity: hypersonic effect. J Neurophysiol 83:3548–3558PubMedGoogle Scholar
  49. Oohashi T, Kawai N, Nishina E et al (2006) The role of biological system other than auditorair-conduction in the emergence of the hypersonic effect. Brain Res 1073–1074:339–347CrossRefPubMedGoogle Scholar
  50. Pang Z, Sakamoto T, Tiwari V, Kim YS, Yang F, Dong X, Güler AD, Guan Y, Caterina MJ (2015) Selective keratinocyte stimulation is sufficient to evoke nociception in mice. Pain 156:656–665CrossRefPubMedGoogle Scholar
  51. Peier AM, Moqrich A, Hergarden AC et al (2002a) A trp channel that senses cold stimuli and menthol. Cell 108:705–715CrossRefPubMedGoogle Scholar
  52. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P, Bevan S, Patapoutian A (2002b) A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046–2049CrossRefPubMedGoogle Scholar
  53. Pruszynski JA, Johansson RS (2014) Edge-orientation processing in first-order tactile neurons. Nat Neurosci 17:1404–1409CrossRefPubMedGoogle Scholar
  54. Sapolsky RM (1996) Why stress is bad for your brain. Science 273:749–750CrossRefPubMedGoogle Scholar
  55. Sato J, Yanai M, Hirao T, Denda M (2000) Water content and thickness of stratum corneum contribute to skin surface morphology. Arch Dermatol Res 292:412–417CrossRefPubMedGoogle Scholar
  56. Sato J, Denda M, Chang S, Elias PM, Feingold KR (2002) Abrupt decreases in environmental humidity induce abnormalities in permeability barrier homeostasis. J Invest Dermatol 119:900–904CrossRefPubMedGoogle Scholar
  57. Sauer GC, Hall JC (1996) Seasonal skin diseases. In: Sauer GC, Hall JC (eds) Manual of skin diseases. Lippincott-Raven, Philadelphia, pp 23–28Google Scholar
  58. Solessio E, Engbretson GA (1993) Antagonistic chromatic mechanisms in photoreceptors of the parietal eye of lizards. Nature 364:442–445CrossRefPubMedGoogle Scholar
  59. Sorrells SF, Caso JR, Munhoz CD, Sapolsky RM (2009) The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 64:33–39CrossRefPubMedPubMedCentralGoogle Scholar
  60. Story GM, Peier AM, Reeve AJ et al (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–829CrossRefPubMedGoogle Scholar
  61. Takei K, Denda S, Kumamoto J, Denda M (2013) Low environmental humidity induces synthesis and release of cortisol in an epidermal organotypic culture system. Exp Dermatol 22:662–664CrossRefPubMedGoogle Scholar
  62. Tsutsumi M, Ikeyama K, Denda S, Nakanishi J, Fuziwara S, Aoki H, Denda M (2009a) Expressions of rod and cone photoreceptor-like proteins in human epidermis. Exp Dermatol 18:567–570CrossRefPubMedGoogle Scholar
  63. Tsutsumi M, Inoue K, Denda S, Ikeyama K, Goto M, Denda M (2009b) Mechanical-stimulation-evoked calcium waves in proliferating and differentiated human keratinocytes. Cell Tissue Res 338:99–106CrossRefPubMedGoogle Scholar
  64. Tsutsumi M, Denda S, Ikeyama K, Goto M, Denda M (2010) Exposure to low temperature induces elevation of intracellular calcium in cultured human keratinocytes. J Invest Dermatol 130:1945–1948CrossRefPubMedGoogle Scholar
  65. Tsutsumi M, Kumamoto J, Denda M (2011) Intracellular calcium response to high temperature is similar in undifferentiated and differentiated cultured human keratinocytes. Exp Dermatol 20:839–840CrossRefPubMedGoogle Scholar
  66. Tsutsumi M, Goto M, Denda M (2013) Dynamics of intracellular calcium in cultured human keratinocytes after localized cell damage. Exp Dermatol 22:367–369CrossRefPubMedGoogle Scholar
  67. Tyring S, Gottlieb A, Papp K, Gordon K, Leonardi C, Wang A, Lalla D, Woolley M, Jahreis A, Zitnik R, Cella D, Krishnan R (2006) Etanercept and clinical outcomes, fatigue, and depression in psoriasis: double-blind placebo-controlled randomised phase III trial. Lancet 367:29–35CrossRefPubMedGoogle Scholar
  68. Wilkinson JD, Rycroft RJ (1992) Contact dermatitis. In: Burton JL, Ebling FJG (eds) Textbook of dermatology, 5th edn. Blackwell Scientific Publications, Oxford, pp 614–615Google Scholar
  69. Wood LC, Jackson SM, Elias PM, Grunfeld C, Feingold KR (1992) Cutaneous barrier perturbation stimulates cytokine production in the epidermis of mice. J Clin Invest 90:482–487CrossRefPubMedPubMedCentralGoogle Scholar
  70. Yagi R, Nishina E, Honda M et al (2003) Modulatory effect of inaudible high-frequency sounds on human acoustic perception. Neurosci Lett 351:191–195CrossRefPubMedGoogle Scholar
  71. Zhao X, Haeseleer F, Fariss RN, Huang J, Baehr W, Milam AH, Palczewski K (1997) Molecular cloning and localization of rhodopsin kinase in the mammalian pineal. Vis Neurosci 114:225–232CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Japan Science and Technology AgencyCRESTKawaguchiJapan
  2. 2.Shiseido Research CenterYokohamaJapan

Personalised recommendations