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Biogerontology

, Volume 2, Issue 4, pp 219–229 | Cite as

Factors of skin ageing share common mechanisms

  • Paolo U. Giacomoni
  • Glen Rein
Article

Abstract

Ageing has been defined as the accumulation of molecular modificationswhich manifest as macroscopic clinical changes. Human skin, unique amongmammalians insofar as it is deprived of fur, is particularly sensitiveto environmental stress. Major environmental factors have beenrecognized to induce modifications of the morphological and biophysicalproperties of the skin. Metabolites from ingested or inhaled substancesdo affect skin, which is also sensitive to endogenous hormone levels.Factors as diverse as ultraviolet radiation, atmospheric pollution,wounds, infections, traumatisms, anoxya, cigarette smoke, and hormonalstatus have a role in increasing the rate of accumulation of molecularmodifications and have thus been termed 'factors of ageing'. All thesefactors share as a common feature, the capability to directly orindirectly induce one of the steps of the micro-inflammatory cycle,which includes the expression of ICAM-1 in endothelial cells. Thistriggers a process leading to the accumulation of damages in the skinresulting in skin ageing since ICAM-1 expression provokes recruitmentand diapedesis of circulating immune cells, which digest theextracellular matrix (ECM) by secreting collagenases, myeloperoxidasesand reactive oxygen species. The activation of these lytic processesprovokes random damage to resident cells, which in turn secreteprostaglandines and leukotrienes. These signaling molecules induce thedegranulation of resident mast cells which release the autacoidhistamine and the cytokine TNF-α thus activating endothelial cellslining adjacent capillaries which release P-selectin and synthesizeICAM-1. This closes a self-maintained micro-inflammatory cycle, whichresults in the accumulation of ECM damage, i.e. skin aging. In thispaper we review the evidence that two factors able to inducemacroscopical and molecular modifications in the skin, protein glycationand stretch, activate the micro-inflammatory cycle. We further presentevidence that three additional factors, two external factors(electromagnetic fields and psychological stressors) and one internalfactor (neuropeptides) also activate the micro-inflammatory cycles andmay therefore be considered as factors of skin ageing.

electromagnetic fields glucose gravity neuropeptides stress 

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References

  1. Ader R (1980) Psychosomatic and psychoimmunologic research. Psychosomatic Med 42: 307-321Google Scholar
  2. Ansel JC, Kaynard AH, Armstrong CA, Olerud J, Bunnett N and Payan D (1996) Skin-nervous system interactions. J Invest Dermatol 106: 198-204PubMedGoogle Scholar
  3. Alstergren P, Ernberg M, Kopp S, Lundeberg T and Theodorsson E (1999) TMJ pain in relation to circulating neuropeptide Y, serotonin, and interleukin-1 beta in rheumatoid arthritis. J Orofac Pain 13: 49-55PubMedGoogle Scholar
  4. Airaksinen KEJ, Salmela PI, Linnaluoto MK, Ikaheimo MJ, Ahola K and Ryhanen LJ (1993) Diminished arterial elasticity in diabetes: association with fluorescent advanced glycosylation end products in collagen Cardiovasc Res 27: 942-945PubMedGoogle Scholar
  5. Anfinogenov VA, Vasil'ev AV, Mymirina IA and Terskikh VV (1991) The interaction of epidermal keratinocytes and fibroblasts during the formation of a live skin equivalent. Tsitologija 34: 60-65Google Scholar
  6. Bjorklund H, Dalsgaard CJ, Jonsson CE and Hermansson A (1986) Sensory and autonomic innervation on non-hairy and hairy human skin. Cell Tissue Res 243: 51-62PubMedGoogle Scholar
  7. Brownlee M, Vlassara H, Kooney T, Ulrich P and Cerami A (1986) Aminoguanidine prevents diabetes-induced arterial wall protein cross-linking. Science 232: 1629-1632PubMedGoogle Scholar
  8. Charonis AS, Reger LA, Dege JE, Kouzi-Koliakos K, Furcht LT, Wohlhueter RM and Tsilibary RC (1990) Laminin alterations after in vitro non-enzymatic glucosylation. Diabetes 39: 807-814PubMedGoogle Scholar
  9. Conrad CD and McEwen BS (2000) Acute stress increases neuropeptide Y mRNA within the arcuate nucleus and hilus of the dentate gyrus. Brain Res Mol Brain Res 79: 102-109PubMedGoogle Scholar
  10. Cossarizza A, Angioni S, Petraglia F, Genazzani AR, Monti D, Capri M, Bersani F, Cadossi R and Franceschi C (1993) Exposure to low-frequency pulsed electromagnetic fields increases interleukin-1 and interleukin-6 production by human peripheral blood mononuclear cells. Exp Cell Res 204: 385-387PubMedGoogle Scholar
  11. Denda M, Tsuchiya T, Elias PM and Feingold KR (2000) Stress alters cutaneous permeability barrier homeostasis Am J Physiol Regul Integr Comp Physiol 278: 367-372Google Scholar
  12. Donnellan M, McKenzie DR and French PW (1997) Effects of exposure to electromagnetic radiation at 835 MHz on growth, morphology and secretory characteristics of a mast cell analogue, RBL-2H3 Cell Biol Int 21: 427-439Google Scholar
  13. Dunn JA, McCance DR, Thorpe SR, Lyons TJ and Baynes JW (1991) Age-dependent accumulation of N(ɛ)-(carboxymethyl) lysine and N(ɛ)-(carboxymethyl)hydroxylysine in human skin collagen. Biochemistry 30: 1205-1210PubMedGoogle Scholar
  14. Dyer DG, Blackledge JA, Katz BM, Hull CJ, Adkisson HD, Thorpe SR, Lyons TJ and Baynes JW (1991) The Maillard reaction in vivo. Z Ernahrungswiss 30: 29-45PubMedGoogle Scholar
  15. Dyer DG, Dunn JA, Thorpe SR, Bailie KE, Lyons TJ, McCance DR and Baynes JW (1993) Accumulation of Maillard reaction products in skin collagen in diabetes and ageing. J Clin Invest 91: 2463-2469PubMedGoogle Scholar
  16. Eastwood M, McGrouther DA and Brown RA (1994) A culture force monitor for measurement of contraction forces generated in human dermal fibroblast cultures: evidence for cell-matrix signaling. Biochem Biophys Acta 120: 186-192Google Scholar
  17. Eastwood M, McGrouther DA and Brown RA (1998) Fibroblast response to mechanical forces. Proc Inst Mech Eng [H] 212: 85-92Google Scholar
  18. Farber EM, Rein G and Lanigan SW (1991) Stress and psoriasis: psychoneuroimmunologic mechanisms. Internat J Dermatol 30: 8-12Google Scholar
  19. Fluck J, Querfeld C, Cremer A, Niland S, Krieg T and Sollberg S (1998) Normal human primary fibroblasts undergo apoptosis in three-dimensional contractile collagen gels. J Invest Dermatol 110: 153-157PubMedGoogle Scholar
  20. Fischer EG, Stingl A and Kirkpatrick CJ (1990) Opioid influence on the adherence of granulocytes to human umbilical vein endothelial cells in vitro. Cell Biol Int Rep 14: 797-804PubMedGoogle Scholar
  21. Forman JC (1987) Substance P and calcitonin gene-related peptide: effects on mast cells and in human skin. Int Archs Allergy Appl Immunol 82: 366-373Google Scholar
  22. Fray TR, Molloy JE, Armitage MP and Sparrow JC (1998) Quantifi-cation of a single human dermal fibroblast contraction Tissue Eng 4: 281-291PubMedGoogle Scholar
  23. Gangi S and Johansson O (2000) A theoretical model based upon mast cell and histamine to explain the recently proclaimed sensitivity to electric and/or magnetic fields in humans. Med Hypotheses 54: 663-671PubMedGoogle Scholar
  24. Garaj-Vrhovac V, Horvat D and Koren Z (1991) The relationship between colony-forming ability, chromosome aberrations and incidence of micronuclei in V79 Chinese hamster cells exposed to microwave radiation. Mutat Res 263: 143-149PubMedGoogle Scholar
  25. Garg A, Chren MM, Sands LP, Matsui MS, Marenus KD, Feingold KR and Elias PM 2001) Psychological stress perturbs epidermal permeability barrier homeostasis: implications for the pathogenesis of stress-associated skin disorders. Arch Dermatol 137: 53-59PubMedGoogle Scholar
  26. Gerra G, Zaimovic A, Zambelli U, Timpano M, Reali N, Bernasconi S and Brambilla F (2000) Neuroendocrine responses to psychological stress in adolescents with anxiety disorder. Neuropsychobiology 42: 82-92PubMedGoogle Scholar
  27. Giacomoni PU (1992) Ageing and cellular defense mechanisms. In: Franceschi C, Crepaldi G, Cristofalo VJ and Vijg J (eds) Ageing and Cellular Defense Mechanisms, Vol 663, pp 1-3. Ann NY Acad SciGoogle Scholar
  28. Giacomoni PU (1995) Radiazione Ultravioletta, Invecchiamento e Blebs. Giornale di Gerontologia 43: 209-210Google Scholar
  29. Giacomoni PU and D'Alessio, P (1996a) Skin ageing: the relevance of anti-oxidants. In: Rattan SIS and Toussaints O (eds) Molecular Gerontology: Research Status and Strategies, pp 177-192. Plenum Press, New YorkGoogle Scholar
  30. Giacomoni PU and D'Alessio P (1996b) Open questions in photobiology IV: photoageing of the skin. J Photochem Photobiol B: Biol 33: 267-272Google Scholar
  31. Giacomoni PU, Declercq L, Hellemans L and Maes D (2000) Ageing of human skin: review of a mechanistic model and first experimental data. IUBMB Life 49: 259-263PubMedGoogle Scholar
  32. Guidi L, Tricerri A, Vangeli M, Frasca D, Riccardo Errani A, Di Giovanni A, Antico L, Menini E, Sciamanna V, Magnavita N, Doria G and Bartoloni C (1999) Neuropeptide Y plasma levels and immunological changes during academic stress. Neuropsychobio 40: 188-195Google Scholar
  33. Hufeland CW (1798) L'Arte di prolungare la vita umana [Italian translation by Luigi Careno]. Vol II, pp 174ff. Eredi di Pietro Galeazzi, PaviaGoogle Scholar
  34. Johansson O, Hilliges M, Bjoernhagen V and Hall K (1994) Skin changes in patients claiming to suffer from 'screen dermatitis': a two-case open-field provocation study. Exp Dermatol 3: 234-238PubMedGoogle Scholar
  35. Johansson O, Hilliges M and Han SW (1996) A screening of skin changes, with special emphasis on neurochemical marker antibody evaluation, in patients claiming to suffer from 'screen dermatitis' as compared to normal healthy controls. Exp Dermatol 5: 279-285PubMedGoogle Scholar
  36. Johnston JA, Taub DD, Lloyd AR, Conlon K, Oppenheim JJ and Kevlin DJ (1994) Human T lymphocyte chemotaxis and adhesion induced by vasoactive intestinal peptide. J Immunol 153: 1762-1768PubMedGoogle Scholar
  37. Kavelaars A, Jeurissen F and Heijnrn CJ (1994) Substance P receptors and signal transduction in leukocytes. Immunomethods 5: 41-48PubMedGoogle Scholar
  38. Kent MJC, Light ND and Bailey AJ (1985) Evidence for glucosemediated covalent cross-linking of collagen after glycosylation in vitro. Biochem J 225: 745-752PubMedGoogle Scholar
  39. Koks S, Mannisto PT, Bourin M, Shlik J, Vasar V and Vasar E (2000) Cholecystokinin-induced anxiety in rats: relevance of pre-experimental stress and seasonal variations. J Psychiatry Neurosci 25: 33-42PubMedGoogle Scholar
  40. Kudielka BM, Schmidt-Reinwald AK, Hellhammer DH and Kirschbaum C (1999) Psychological and endocrine responses to psychosocial stress and dexamethasone/corticotropin-releasing hormone in healthy postmenopausal women and young controls. Neuroendocrinology 70: 422-430PubMedGoogle Scholar
  41. Kunt T, Forst T, Harzer O, Buchert G, Pfutzner A, Lobig M, Zschabitz A, Stofft E, Engelbach M and Beyer J (1998) The influence of advanced glycation endproducts (AGE) on the expression of human endothelial adhesion molecules. Exp Clin Endocrinol Diabetes 106: 183-188PubMedGoogle Scholar
  42. Lamb RG, Harper CC, McKinney JS, Rzigalinski BA and Ellis EF (1997) Alterations in phosphatidylcholine metabolism of stretchinjured cultured rat astrocytes. J Neurochem 68: 1904-1910PubMedGoogle Scholar
  43. Maes A, Verschaeve L, Arroyo A, De Wagter C and Vercruyssen L (1993) In vitro cytogenetic effects of 2450 MHz waves on human periferal blood lymphocytes. Bioelectromagnetics 1: 495-501Google Scholar
  44. Matis WL, Lavker RM and Murphy GF (1990) Substance P induces the expression of an endothelial-leukocyte adhesion molecule by microvascular endothelium. J Invest Dermatol 94: 492-498PubMedGoogle Scholar
  45. McKinney JS, Willoughby KA, Liang S and Ellis EF (1996) Stretchinduced injury of cultured neural, glial and endothelial cells. Effect of polyethylene glycol-conjugated superoxide dismutase. Stroke 27: 934-940PubMedGoogle Scholar
  46. Melling M, Pfeiler W, Karimian-Teherani D, Schnallinger M, Sobal G, Zangerle C and Menzel EJ (2000) Differential scanning calorimetry, biochemical and biomechanical analysis of human skin from individual with diabetes mellitus Anat Rec 259: 327-333PubMedGoogle Scholar
  47. Mizutari K, Ono T, Ikeda K, Kayashima K and Horiuchi S (1997) Photo-enhanced modification of human skin elastin in actinic elastosis by N (ɛ)-carboxymethyl)lysine, one of the glycoxidation products of the Maillard reaction. J Invest Dermatol 108: 797-802PubMedGoogle Scholar
  48. Monnier V and Cerami A (1983) Detection of nonenzymatic browning products in the human lens Biochem Biophys Acta 760: 97-103PubMedGoogle Scholar
  49. Monnier VM, Sell DR, Abdul-Karim FW and Emancipator SN (1988) Collagen browning and cross linking are increased in chronic experimental hyperglycemia: relevance to diabetes and ageing. Diabetes 37: 867-872PubMedGoogle Scholar
  50. Morandi MA, Del Rio JA, Caren RP and Caren LD (1994) Effects of short term exposure to 60 Hz electromagnetic fields on interleukin 1 and interleukin 6 production by peritoneal exudate cells. Life Sci 54: 731-738PubMedGoogle Scholar
  51. Morgan CA, Wang S, Southwick SM, Rasmusson A, Hazlett G, Hauger RI and Charney DS (2000) Plasma neuropeptide-Y concentrations in humans exposed to military survival training. Biol Psychiatry 47: 902-909PubMedGoogle Scholar
  52. Mousa SA, Machelska H, Schafer M and Stein C (2000) Coexpression of beta-endorphin with adhesion molecules in a model of inflammatory pain. J Neuroimmunol 108: 160-170PubMedGoogle Scholar
  53. Nakagawa N, Iwamoto I and Yoshida S (1993) Effect of substance P on the expression of an adhesion molecule ICAM-1 in human vascular endothelial cells. Regul Pept 46: 223-224PubMedGoogle Scholar
  54. Odetti PR, Borgoglio A and Rolandi R (1992) Age-related increase of collagen fluorescence in human sub-cutaneous tissue. Metabolism 41: 655-658PubMedGoogle Scholar
  55. Oehme P, Hecht K, Faulhaber HD, Nieber K, Roske I and Rathsack R (1987) Relationship of substance P to catecholamines, stress and hypertension. J Cardiovasc Pharmacol Suppl 12: S109-S111.Google Scholar
  56. Ortega E, Forner MA and Barriga C (1996) Effect of beta-endorphin on adherence, chemotaxic and phagocytosis of Candida Albicans by peritoneal macrophages. Comp Immunol Microbiol Infect Dis 19: 267-274PubMedGoogle Scholar
  57. Payan D, Brewster D and Goetzl E (1993) Specific stimulation of human T lymphocytes by substance P. J Immunol 131: 1613-1615Google Scholar
  58. Quinlan KL, Song IS, Bunnett NW, Letran E, Steinhoff M, Harten B, Olerud JE, Armstrong CA, Wright Caughman S and Ansel JC (1998) Neuropeptide regulation of human dermal microvascular endothelial cell ICAM-1 expression and function. Am J Physiol 275: C1580-C1590PubMedGoogle Scholar
  59. Quinlan KL, Naik SM, Cannon G, Armstrong CA, Bunnett NW, Ansel JC and Caughman SW (1999) Substance P activates coincident NF-AT-and NF-kappa B-dependent adhesion molecule gene expression in microvascular endothelial cells 229 through intracellular calcium mobilization. J Immunol 163: 5656-5665PubMedGoogle Scholar
  60. Raud J, Lundeberg T, Brodda-Jansen G et al. (1991) Potent antiinflammatory action of calcitonin-gene-related peptide. Biochem Biophys Res Comm 180: 1429-1435PubMedGoogle Scholar
  61. Ren J, Goa J, Ojeas H, Lightfoot SA, Kida M, Brewer K and Harty RF (2000) Involvement of capsaicin-sensitive sensory neurons in stress-induced gastroduodenal mucosal injury in rats. Dig Dis Sci 45: 830-836PubMedGoogle Scholar
  62. Robert L and Labat-Robert J (2000) Ageing of connective tissues: from genetic to epigenetic mechanisms. Biogenrontology 1: 123-131Google Scholar
  63. Rupniak NM, Carlson EC, Harrison T, Oates B, Seward E, Owen S, deFelipe C, Hunt S and Wheeldon A (2000) Pharmacological blockade or genetic deletion of substance P (NK(1)) receptors attenuates neonatal vocalisation in guinea-pigs and mice. Neuropharmacology 39: 1413-1421PubMedGoogle Scholar
  64. Rzigalinski BA, Weber JT, Willoughby KA and Ellis EF (1998) Intracellular free calcium dynamics in stretch-injured astrocytes. J Neurochem 70: 2377-2385PubMedGoogle Scholar
  65. Singh LK, Pang X, Alexacos N, Letourneau R and Theoharides TC (1999) Acute immobilization stress triggers skin mast cell degranulation via corticotropin releasing hormone, neurotensin, and substance P: a link to neurogenic skin disorders. Brain Behav Immunol 13: 225-239Google Scholar
  66. Slominski A, Wortsman J, Luger T, Paus R and Solomon S (2000) Corticotropin releasing hormone and proopiomelanocortin involvement in the cutaneous response to stress. Physiol Rev 80: 979-1020PubMedGoogle Scholar
  67. Smith CH, Barker JN, Morris RW, MacDonald DM and Lee TH (1993) Neuropeptides induce rapid expression of endothelial cell adhesion molecules and elicit granulocytic infiltration in human skin. J Immunol 151: 3274-3282PubMedGoogle Scholar
  68. Steplewski Z and Vogel HW 1986) Total leukocytes, T cell subpopulation and natural killer (NK) activity in rats exposed to restraint stress. Life Sci 38: 2419-2425PubMedGoogle Scholar
  69. Sung CP, Arleth AJ and Feuerstein GZ (1991) Neuropeptide Y upregulates the adhesiveness of human endothelial cells for leukocytes. Circ Res 68: 314-318PubMedGoogle Scholar
  70. Sung CP, Arleth AJ, Aiyar N, Bhatnagar PK, Lysko PG and Feuerstein G (1992) CGRP stimulates the adhesion of leukocytes to vascular endothelial cells. Peptides 13: 429-435PubMedGoogle Scholar
  71. Tanaka S, Avigad G, Brodsky B and Eikenberry EF (1988) Glycation induces expansion of the molecular packing of collagen. J Mol Biol 203: 495-505PubMedGoogle Scholar
  72. Teofoli P, Frezzolini A, Puddu P, De Pita O, Mauviel A and Lotti T (1999) The role of proopiomelanocortin-derived peptides in skin fibroblasts and mast cell functions. Ann NY Acad Sci 885: 268-276PubMedGoogle Scholar
  73. Tominaga K, Honda K, Akahoshi A, Makino Y, Kawarabayashi T, Takano Y and Kamiya H (1999) Substance P causes adhesion of neutrophils to endothelial cells via protein kinase C. Biol Pharm Bull 22: 1242-1245PubMedGoogle Scholar
  74. Tsilibary EC, Charonis AS, Reger LA, Wohlhueter RM and Furcht LT (1988) The effect of non enzymatic glycosylation on the binding of the non collagenous NC1 domain to collagen IV. J Biol Chem 263: 4302-4308PubMedGoogle Scholar
  75. Verzijl N, DeGroot J, Thorpe SR, Bank RA, Shaw JN, Lyons TJ, Bijlsma JW, Lafeber FP, Baynes JW and Te Koppele JM (2000) Effect of collagen turnover on the accumulation of advanced glycation endproducts. J Biol Chem 275: 39027-39031PubMedGoogle Scholar
  76. Vishwanath R and Mukherjee R (1996) Substance P promotes lymphocyte-endothelial cell adhesion preferentially via LFA-1/ICAM-1 interactions. J Neuroimmunol 71: 163-171PubMedGoogle Scholar
  77. Vishwanath V, Frank KE, Elmets CA, Dauchot PJ and Monnier VM (1986) Glycation of skin collagen in type I diabetes mellitus. Correlation with long-term complications Diabetes 35: 916-921Google Scholar
  78. Vlassara H, Valinsky J, Brownlee M, Cerami C, Nishimoto S and Cerami A (1987) Advanced glycosylation end products on erythrocyte cell surface induce receptor-mediated phagocytosis by macrophages. A model for turnover of ageing cells. J Exp Med 166: 539-549PubMedGoogle Scholar
  79. Vlassara H, Fuh H, Donnelly T and Cybulsky M (1995) Advanced glycation endproducts promote adhesion molecule (VCAM-1, ICAM-1) expression and atheroma formation in normal rabbits Mol Med 1: 447-456Google Scholar
  80. Wallengren J (1997) Vasoactive peptides in the skin. J Investig Dermatol Symp Proc 2: 49-55PubMedGoogle Scholar
  81. Williams G, Cardoso H, Ball JA, Mulderry PK, Cooke E and Bloom SR (1988) Potent and comparable vasodilator action of A-and Bcalcitonin gene related peptides on the superficial subcutaneous vasculature of man. Clin Sci 75: 309-313PubMedGoogle Scholar
  82. Wintzen M, Zanello SB, Holick MF, Wiegant VM, Burbach JP and Vermeer BJ (2000) Condition-dependent presence of betalipotropin-like peptide in human keratinocytes. Peptides 21: 691-697PubMedGoogle Scholar
  83. Xu IS, Luo L, Ji, RR, Hokfelt T, Xu XJ and Wiesenfeld-Hallin Z (1998) The effect of intrathecal neuropeptide Y on the flexor reflex in rats after carrageenan-induced inflammation. Neuropeptides 32: 447-452PubMedGoogle Scholar
  84. Zanello SB, Jackson DM and Holick MF (1999) An immunocytochemical approach to the study of beta-endorphin production in human keratinocytes using confocal microscopy. Ann NY Acad Sci 885: 85-99PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Paolo U. Giacomoni
    • 1
  • Glen Rein
    • 2
  1. 1.Clinique LaboratoriesMelvilleUSA
  2. 2.Estee Lauder Research ParkMelvilleUSA

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