Neuropeptides in the skin: interactions between the neuroendocrine and the skin immune systems

Abstract: The interaction between components of the nervous system and multiple target cells in the cutaneous immune system has been receiving increasing attention. It has been observed that certain skin diseases such as psoriasis and atopic dermatitis have a neurogenic component. Neuropeptides released by sensory nerves that innervate the skin and often contact epidermal and dermal cells can directly modulate functions of keratinocytes, Langerhans cells (LC), mast cells, dermal microvascular endothelial cells and infiltrating immune cells. Among these neuropeptides the tachykinins substance P (SP) and neurokinin A (NKA), calcitonin gene related peptide (CGRP), vasoactive intestinal peptide (VIP) and somato statin (SOM) have been reported to effectively modulate skin and immune cell functions such as cell proliferation, cytokine production or antigen presentation under physiological or pathophysiological conditions. Expression and regulation of their corresponding receptors that are expressed on a variety of skin cells as well as the presence of neuropeptidespecific peptidases such as neutral endopeptidase (NEP) or angiotensinconverting enzyme (ACE) determine the final biological response mediated by these peptides on the target cell or tissue. Likewise, skin cells like keratinocytes or fibroblasts are a source for neurotrophins such as nerve growth factor that are required not only for survival and regeneration of sensory neurons but also to control responsiveness of these neurons to external stimuli. Therefore, neuropeptides, neuropeptide receptors, neuropeptidedegrading enzymes and neurotrophins participate in a complex, interdependent network of mediators that modulate skin inflammation, wound healing and the skin immune system. This review will focus on recent studies demonstrating the role of tachykinins, CGRP, SOM and VIP and their receptors and neuropeptide‐degrading enzymes in mediating neurogenic inflammation in the skin.

[1]  W. Ho,et al.  Human monocytes and macrophages express substance P and neurokinin-1 receptor. , 1997, Journal of immunology.

[2]  J. Streilein,et al.  Calcitonin gene-related peptide is necessary for ultraviolet B-impaired induction of contact hypersensitivity. , 1997, Journal of immunology.

[3]  J. Bauer,et al.  The neuropeptide substance P activates transcription factor NF-kappa B and kappa B-dependent gene expression in human astrocytoma cells. , 1997, Journal of immunology.

[4]  D. Julius,et al.  The capsaicin receptor: a heat-activated ion channel in the pain pathway , 1997, Nature.

[5]  M. Rosenblatt,et al.  Inhibitory effect of calcitonin gene-related peptide on myometrial contractility is diminished at parturition. , 1997, Endocrinology.

[6]  C. Estrada,et al.  Neuronal Nitric Oxide Synthase Activation by Vasoactive Intestinal Peptide in Bovine Cerebral Arteries , 1997, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[7]  C. Souchier,et al.  Presence of somatostatin in normal human epidermis , 1997, The British journal of dermatology.

[8]  T. Luger,et al.  Human dermal microvascular endothelial cells express the melanocortin receptor type 1 and produce increased levels of IL-8 upon stimulation with alpha-melanocyte-stimulating hormone. , 1997, Journal of immunology.

[9]  R. Funk,et al.  Immunohistochemical detection of human skin nerve fibers. , 1997, Acta Histochemica.

[10]  M. Green,et al.  The epidermal nerve fibre network: characterization of nerve fibres in human skin by confocal microscopy and assessment of racial variations , 1997, The British journal of dermatology.

[11]  D. Payan,et al.  The control of microvascular permeability and blood pressure by neutral endopeptidase , 1997, Nature Medicine.

[12]  Jun-ya Asai,et al.  Reduction of the DTH response is related to morphological changes of Langerhans cells in mice exposed to acute immobilization stress , 1997, Clinical and experimental immunology.

[13]  R. Quirion,et al.  A potent and selective CGRP2 agonist, ys(Et)2,7]hCGRPα: comparison in prototypical CGRP1 and CGRP2 in vitro ioassays , 1997 .

[14]  U. Hipler,et al.  Vasoactive intestinal peptide supports induced migration of human keratinocytes and their colonization of an artificial polyurethane matrix , 1997, Regulatory Peptides.

[15]  G. Calo’,et al.  Neurokinin Receptors , 1997, Annals of the New York Academy of Sciences.

[16]  L. Edvinsson,et al.  Release of Histamine from Dural Mast Cells by Substance P and Calcitonin Gene-Related Peptide , 1997, Cephalalgia : an international journal of headache.

[17]  T. Luger,et al.  Evidence for the differential expression of the functional alpha-melanocyte-stimulating hormone receptor MC-1 on human monocytes. , 1997, Journal of immunology.

[18]  S. Eichmüller,et al.  A simple immunofluorescence technique for simultaneous visualization of mast cells and nerve fibers reveals selectivity and hair cycle – dependent changes in mast cell – nerve fiber contacts in murine skin , 1997, Archives of Dermatological Research.

[19]  L. Misery,et al.  Binding and in vitro modulation of human epidermal Langerhans cell functions by substance P , 1997, Archives of Dermatological Research.

[20]  D. Payan,et al.  Substance P and bradykinin stimulate plasma extravasation in the mouse gastrointestinal tract and pancreas. , 1997, The American journal of physiology.

[21]  D. Pozo,et al.  Characterization of VIP receptor-effector system antagonists in rat and mouse peritoneal macrophages. , 1997, European journal of pharmacology.

[22]  J. M. Lipton,et al.  Anti-inflammatory actions of the neuroimmunomodulator α-MSH , 1997 .

[23]  S. Fujimoto,et al.  Weibel‐Palade bodies as a storage site of calcitonin gene‐related peptide and endothelin‐1 in blood vessels of the rat carotid body , 1997, The Anatomical record.

[24]  D. Payan,et al.  Identification of Potential Tyrosine-containing Endocytic Motifs in the Carboxyl-tail and Seventh Transmembrane Domain of the Neurokinin 1 Receptor* , 1997, The Journal of Biological Chemistry.

[25]  A. Couvineau,et al.  Aspartate 196 in the first extracellular loop of the human VIP1 receptor is essential for VIP binding and VIP-stimulated cAMP production. , 1997, Biochemical and biophysical research communications.

[26]  M. Ichinose,et al.  Enhancement of phagocytosis by calcitonin gene-related peptide (CGRP) in cultured mouse peritoneal macrophages , 1996, Peptides.

[27]  S. Dobson,et al.  Regulation of VIP and other Neuropeptides by c‐Jun in Sensory Neurons: Implications for the Neuropeptide Response to Axotomy , 1996, The European journal of neuroscience.

[28]  K. Nordlind,et al.  Vasoactive Intestinal Polypeptide Inhibits the Established Allergic Contact Dermatitis in Humans a , 1996, Annals of the New York Academy of Sciences.

[29]  M. Sharif,et al.  Substance P-induced mitogenesis in human astrocytoma cells correlates with activation of the mitogen-activated protein kinase signaling pathway. , 1996, Cancer research.

[30]  S. Scherer,et al.  Chromosomal localization in mouse and human of the vasoactive intestinal peptide receptor type 2 gene: a possible contributor to the holoprosencephaly 3 phenotype. , 1996, Genomics.

[31]  A. Neely,et al.  Recombinant neutral endopeptidase decreases oedema in the skin of burned guinea-pigs. , 1996, Burns : journal of the International Society for Burn Injuries.

[32]  B. Gilchrest,et al.  Innervation of melanocytes in human skin , 1996, The Journal of experimental medicine.

[33]  A. Kagey‐Sobotka,et al.  Substance P activates the release of histamine from human skin mast cells through a pertussis toxin-sensitive and protein kinase C-dependent mechanism. , 1996, Clinical immunology and immunopathology.

[34]  J. Lakkakorpi,et al.  QUANTITATIVE HISTOCHEMICAL ANALYSIS OF MAST CELLS AND SENSORY NERVES IN PSORIATIC SKIN , 1996, The Journal of pathology.

[35]  R. Coggeshall,et al.  Localization and activation of substance P receptors in unmyelinated axons of rat glabrous skin , 1996, Brain Research.

[36]  U. Höpken,et al.  Neurogenic Amplification of Immune Complex Inflammation , 1996, Science.

[37]  M. Wintzen.  Corrections to "Proopiomelanocortin, Its Derived Peptides, and the Skin" , 1996 .

[38]  N. Vaysse,et al.  Molecular mechanisms of antiproliferative effect of somatostatin: involvement of a tyrosine phosphatase. , 1996, Metabolism: clinical and experimental.

[39]  L. Edvinsson,et al.  Calcitonin Gene-Related Peptide is Released from Capsaicin-Sensitive Nerve Fibres and Induces Vasodilatation of Human Cerebral Arteries Concomitant with Activation of Adenylyl Cyclase , 1996, Cephalalgia : an international journal of headache.

[40]  M. Montminy,et al.  Regulation of somatostatin gene transcription by cyclic adenosine monophosphate. , 1996, Metabolism: clinical and experimental.

[41]  L. Malinovský.  Sensory nerve formations in the skin and their classification , 1996, Microscopy research and technique.

[42]  N. Aiyar,et al.  A cDNA Encoding the Calcitonin Gene-related Peptide Type 1 Receptor (*) , 1996, The Journal of Biological Chemistry.

[43]  B. Roos,et al.  Identification of a protein that confers calcitonin gene-related peptide responsiveness to oocytes by using a cystic fibrosis transmembrane conductance regulator assay. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[44]  J. Cohen,et al.  Neuropeptides induce release of nitric oxide from human dermal microvascular endothelial cells. , 1996, The Journal of investigative dermatology.

[45]  Y. Aragane,et al.  Pro-opiomelanocortin-derived peptides induce IL-10 production in human monocytes. , 1996, Journal of immunology.

[46]  C. Wiedermann,et al.  Induction of endothelial cell differentiation into capillary-like structures by substance P. , 1996, European journal of pharmacology.

[47]  G. Girolomoni,et al.  Epidermal cytokine and neuronal peptide modulation of contact hypersensitivity reactions. , 1996, Immunopharmacology.

[48]  K. Nordlind,et al.  Inhibitory effect of vasoactive intestinal polypeptide and ketanserin on established allergic contact dermatitis in man. , 1996, Acta Dermato-Venereologica.

[49]  N. Bunnett,et al.  Mechanisms of desensitization and resensitization of G protein-coupled neurokinin1 and neurokinin2 receptors. , 1996, Molecular pharmacology.

[50]  D. McDonald,et al.  Substance P (NK1) receptor immunoreactivity on endothelial cells of the rat tracheal mucosa. , 1996, The American journal of physiology.

[51]  M. Fournié-Zaluski,et al.  Effects of angiotensin-converting enzyme and neutral endopeptidase inhibitors: influence of bradykinin. , 1996, European journal of pharmacology.

[52]  M. Simon,et al.  alpha-Melanocyte-stimulating hormone induces hapten-specific tolerance in mice. , 1996, Journal of immunology.

[53]  E. Fleck,et al.  Activation of adenylate cyclase and phosphodiesterase inhibition enhance neutral endopeptidase activity in human endothelial cells , 1995, Peptides.

[54]  F. Fantini,et al.  Neurochemical markers in human cutaneous Merkel cells , 1995, Experimental dermatology.

[55]  S. Grabbe,et al.  Modulation of Langerhans cell function by epidermal nerves. , 1995, The Journal of allergy and clinical immunology.

[56]  D. Gawkrodger,et al.  Neuropeptides and general neuronal marker in psoriasis an immunohistochemical study , 1995, Clinical and experimental dermatology.

[57]  C. Maggi,et al.  The mammalian tachykinin receptors. , 1995, General pharmacology.

[58]  G. Rayan,et al.  Vasoactive intestinal peptide and nerve growth factor effects on nerve regeneration. , 1995, The Journal of the Oklahoma State Medical Association.

[59]  P. Holzer,et al.  Diverse interactions of calcitonin gene related peptide and nitric oxide in the gastric and cutaneous microcirculation. , 1995, Canadian Journal of Physiology and Pharmacology.

[60]  U. McGovern,et al.  Intracellular calcium as a second messenger following growth stimulation of human keratinocytes , 1995, The British journal of dermatology.

[61]  L. F. Kolakowski,et al.  Neutral endopeptidase modulation of septic shock , 1995, The Journal of experimental medicine.

[62]  F. Gillardon,et al.  Calcitonin gene-related peptide, substance P and nitric oxide are involved in cutaneous inflammation following ultraviolet irradiation. , 1995, European journal of pharmacology.

[63]  N. Aiyar,et al.  Cloning and functional characterization of the human vasoactive intestinal peptide (VIP)-2 receptor. , 1995, Biochemical and biophysical research communications.

[64]  S. Beissert,et al.  Inhibition of the induction of delayed-type and contact hypersensitivity by calcitonin gene-related peptide. , 1995, Journal of immunology.

[65]  M. Hilliges,et al.  Histaminergic nerves demonstrated in the skin. A new direct mode of neurogenic inflammation? , 1995, Experimental dermatology.

[66]  E. Goetzl,et al.  Structure, expression, and chromosomal localization of the type I human vasoactive intestinal peptide receptor gene. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[67]  D. Hoyer,et al.  Classification and nomenclature of somatostatin receptors. , 1995, Trends in pharmacological sciences.

[68]  A. Harmar,et al.  Molecular characterisation of novel receptors for PACAP and VIP. , 1995, Biochemical Society Transactions.

[69]  J. Fauchère,et al.  Receptors and antagonists for substance P and related peptides. , 1994, Pharmacological reviews.

[70]  S. Kondo,et al.  Interleukin-10 inhibits the elicitation phase of allergic contact hypersensitivity. , 1994, The Journal of investigative dermatology.

[71]  G. Wendelschafer‐Crabb,et al.  Innervation and vasculature of human sweat glands: an immunohistochemistry-laser scanning confocal fluorescence microscopy study , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[72]  C. Shaw,et al.  The regional distribution of neuropeptides in human skin as assessed by radioimmunoassay and high‐performance liquid chromatography , 1994, Clinical and experimental dermatology.

[73]  D. Payan,et al.  Agonist-induced internalization of the substance P (NK1) receptor expressed in epithelial cells. , 1994, The Biochemical journal.

[74]  S. Collins,et al.  Fourth isoform of preprotachykinin messenger RNA encoding for substance P in the rat intestine. , 1994, Biochemical and biophysical research communications.

[75]  J. Vishwanatha,et al.  Effects of smokeless tobacco on chemically transformed hamster oral keratinocytes: role of angiotensin I-converting enzyme. , 1994, Carcinogenesis.

[76]  D. Payan,et al.  Interactions between neutral endopeptidase (EC 3.4.24.11) and the substance P (NK1) receptor expressed in mammalian cells. , 1994, The Biochemical journal.

[77]  D. Payan,et al.  Stimulation of transcriptional regulatory activity by substance P. , 1994, Neuroimmunomodulation.

[78]  P. Gressens,et al.  Distribution of VIP mRNA and two distinct VIP binding sites in the developing rat brain: Relation to ontogenic events , 1994, The Journal of comparative neurology.

[79]  A. Enk,et al.  Induction of hapten-specific tolerance by interleukin 10 in vivo , 1994, The Journal of experimental medicine.

[80]  G. Bell,et al.  Stimulation of tyrosine phosphatase and inhibition of cell proliferation by somatostatin analogues: mediation by human somatostatin receptor subtypes SSTR1 and SSTR2. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[81]  A. Szallasi,et al.  The vanilloid (capsaicin) receptor: receptor types and species differences. , 1994, General pharmacology.

[82]  A. Ohkawara,et al.  Substance P induces inositol 1,4,5‐trisphosphate and intracellular free calcium increase in cultured normal human epidermal keratinocytes , 1994, Experimental dermatology.

[83]  J. Warren,et al.  Opposing roles of cyclic AMP in the vascular control of edema formation , 1993, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[84]  D. Lombardo,et al.  Characterization of the oligosaccharide moiety of VIP receptor from the human pancreatic cell line BxPC-3 , 1993, Peptides.

[85]  S. Nakanishi,et al.  Direct effects of cutaneous neuropeptides on adenylyl cyclase activity and proliferation in a keratinocyte cell line: stimulation of cyclic AMP formation by CGRP and VIP/PHM, and inhibition by NPY through G protein-coupled receptors. , 1993, The Journal of investigative dermatology.

[86]  J. Grider,et al.  Expression of functional receptors for vasoactive intestinal peptide in freshly isolated and cultured gastric muscle cells , 1993, Regulatory Peptides.

[87]  D. Macdonald,et al.  Neuropeptides induce rapid expression of endothelial cell adhesion molecules and elicit granulocytic infiltration in human skin. , 1993, Journal of immunology.

[88]  A. Kaynard,et al.  Neurokinin modulation of normal human keratinocyte cytokine production , 1993 .

[89]  D. Eedy,et al.  Neuropeptides in skin , 1993, The British journal of dermatology.

[90]  U. Otten,et al.  Nerve growth factor (NGF) regulates tachykinin gene expression and biosynthesis in rat sensory neurons during early postnatal development , 1993, Neuropeptides.

[91]  J. Brown,et al.  Substance P selectively activates TNF-alpha gene expression in murine mast cells. , 1993, Journal of immunology.

[92]  S. Grabbe,et al.  Regulation of Langerhans cell function by nerves containing calcitonin gene-related peptide , 1993, Nature.

[93]  Z. Abdel‐Malek,et al.  The Expression of Proopiomelanocortin and Various POMC‐Derived Peptides in Mouse and Human Skin , 1993, Annals of the New York Academy of Sciences.

[94]  D. Payan,et al.  Downregulation of neutral endopeptidase (EC 3.4.24.11) in the inflamed rat intestine. , 1993, American Journal of Physiology.

[95]  M. Hilliges,et al.  Somatostatin-like immunoreactivity is found in dendritic guard cells of human sweat ducts , 1993, Peptides.

[96]  D. Leszczyński,et al.  Angiopeptin, the octapeptide analogue of somatostatin, decreases rat heart endothelial cell adhesiveness for mononuclear cells , 1993, Regulatory Peptides.

[97]  M. Mitsuhashi,et al.  Multiple intracellular signaling pathways of the neuropeptide substance P receptor , 1992, Journal of neuroscience research.

[98]  D. Jacobowitz,et al.  Distribution of Calcitonin Gene—Related Peptide in the Central Nervous System of the Rat by Immunocytochemistry and in Situ Hybridization Histochemistry a , 1992, Annals of the New York Academy of Sciences.

[99]  C. Sternini.  Enteric and Visceral Afferent CGRP Neurons , 1992 .

[100]  N. Aiyar,et al.  CGRP stimulates the adhesion of leukocytes to vascular endothelial cells , 1992, Peptides.

[101]  A. Giannetti,et al.  Substance P is diminished and vasoactive intestinal peptide is augmented in psoriatic lesions and these peptides exert disparate effects on the proliferation of cultured human keratinocytes. , 1992, The Journal of investigative dermatology.

[102]  G. Girolomoni,et al.  Peptidergic Neurons and Vasoactive Intestinal Peptide Modulate Experimental Delayed‐Type Hypersensitivity Reactions a , 1992, Annals of the New York Academy of Sciences.

[103]  K. Bost,et al.  Modulation of the mRNAs encoding substance P and its receptor in rat macrophages by LPS. , 1992, Regional immunology.

[104]  S. Nakanishi,et al.  Molecular Characterization of the Three Tachykinin Receptors , 1991, Annals of the New York Academy of Sciences.

[105]  C. Sternini.  Enteric and visceral afferent CGRP neurons: Targets of innervation and differential expression patterns , 1991, Regulatory Peptides.

[106]  P. Holzer.  Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons. , 1991, Pharmacological reviews.

[107]  S. Brain,et al.  Inflammatory edema induced by interactions between IL-1 and the neuropeptide calcitonin gene-related peptide. , 1991, Journal of immunology.

[108]  M. Goebeler,et al.  Neuropeptides enhance irritant and allergic contact dermatitis. , 1991, The Journal of investigative dermatology.

[109]  J. Kessler,et al.  Cytokine regulation of substance P expression in sympathetic neurons. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[110]  J. Wallengren.  Substance P antagonist inhibits immediate and delayed type cutaneous hypersensitivity reactions , 1991, The British journal of dermatology.

[111]  M. Zimmermann,et al.  Ultraviolet irradiation of the skin attenuates calcitonin gene-related peptide mRNA expression in rat dorsal root ganglion cells , 1991, Neuroscience Letters.

[112]  D. Gruenert,et al.  Glucocorticoids induce neutral endopeptidase in transformed human tracheal epithelial cells. , 1991, The American journal of physiology.

[113]  S. Nakanishi,et al.  Selective inhibition of expression of the substance P receptor mRNA in pancreatic acinar AR42J cells by glucocorticoids. , 1990, The Journal of biological chemistry.

[114]  A. Neely,et al.  Hageman factor-dependent kinin activation in burns and its theoretical relationship to postburn immunosuppression syndrome and infection. , 1990, The Journal of burn care & rehabilitation.

[115]  A. Schally,et al.  Antitumor effects of somatostatin mediated by the stimulation of tyrosine phosphatase. , 1990, Metabolism: clinical and experimental.

[116]  G. Girolomoni,et al.  Capsaicin-sensitive primary sensory neurons are potent modulators of murine delayed-type hypersensitivity reactions. , 1990, Journal of immunology.

[117]  C. Shaw,et al.  Vasoactive intestinal peptide (VIP) and peptide histidine methionine (PHM) in human eccrine sweat glands: demonstration of innervation, specific binding sites and presence in secretions , 1990, The British journal of dermatology.

[118]  E. Theodorsson,et al.  Tachykinins and calcitonin gene-related peptide in oxazolone-induced allergic contact dermatitis in mice. , 1990, The Journal of investigative dermatology.

[119]  S. Seidenari,et al.  Neuropeptides in skin from patients with atopic dermatitis: an immunohistochemical study , 1990, The British journal of dermatology.

[120]  C. Maggi,et al.  NK1‐receptors mediate the proliferative response of human fibroblasts to tachykinins , 1990, British journal of pharmacology.

[121]  A. Haegerstrand,et al.  Calcitonin gene-related peptide stimulates proliferation of human endothelial cells. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[122]  A. Haegerstrand,et al.  Vasoactive intestinal polypeptide stimulates cell proliferation and adenylate cyclase activity of cultured human keratinocytes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[123]  Z. Werb,et al.  Phorbol diesters regulate expression of the membrane neutral metalloendopeptidase (EC 3.4.24.11) in rabbit synovial fibroblasts and mammary epithelial cells. , 1989, The Journal of biological chemistry.

[124]  D. McDonald,et al.  Neutral endopeptidase and neurogenic inflammation in rats with respiratory infections. , 1989, Journal of applied physiology.

[125]  J. Changeux,et al.  Calcitonin gene-related peptide and cyclic AMP stimulate phosphoinositide turnover in skeletal muscle cells. Interaction between two second messenger systems. , 1989, The Journal of biological chemistry.

[126]  H. Möller,et al.  Some neuropeptides as modulators of experimental contact allergy , 1988, Contact dermatitis.

[127]  K. Sato,et al.  Effect of VIP on sweat secretion and cAMP accumulation in isolated simian eccrine glands. , 1987, The American journal of physiology.

[128]  B. Coventry,et al.  Two immunohistochemically identified populations of calcitonin gene-related peptide (CGRP)-immunoreactive axons in human skin , 1987, Brain Research.

[129]  D. Payan,et al.  Distribution of somatostatin receptors on murine spleen and Peyer's patch T and B lymphocytes , 1987, Brain, Behavior, and Immunity.

[130]  F. Sundler,et al.  Occurrence and distribution of neuropeptides in the human skin. An immunocytochemical and immunochemical study on normal skin and blister fluid from inflamed skin. , 1987, Acta dermato-venereologica.

[131]  D. Regoli,et al.  Pharmacological receptors for substance P and neurokinins. , 1987, Life sciences.

[132]  S. Said,et al.  Receptors for vasoactive intestinal peptide on isolated human sweat glands , 1986, Peptides.

[133]  Timothy J. Williams,et al.  Potent vasodilator activity of calcitonin gene-related peptide in human skin. , 1986, The Journal of investigative dermatology.

[134]  R. Smallridge,et al.  Angiotensin-converting enzyme: characteristics in human skin fibroblasts. , 1986, Metabolism: clinical and experimental.

[135]  O. Johansson.  On the occasion of the 20th Anniversary of the Stockholm ‘Amine Group’, November 1985. , 1986 .

[136]  L. Swanson,et al.  Expression in brain of a messenger RNA encoding a novel neuropeptide homologous to calcitonin gene-related peptide. , 1985, Science.

[137]  E. G. Erdös,et al.  Neutral metalloendopeptidase in human lung tissue and cultured cells. , 1985, The American review of respiratory disease.

[138]  C. Dalsgaard,et al.  Stimulation of connective tissue cell growth by substance P and substance K , 1985, Nature.

[139]  O. Johansson.  Morphological Characterization of the Somatostatin‐Immunoreactive Dendritic Skin Cells in Urticaria Pigmentosa Patients by Computerized Image Analysis , 1985, Scandinavian journal of immunology.

[140]  E. Goetzl,et al.  Inhibition by somatostatin of the release of mediators from human basophils and rat leukemic basophils. , 1984, Journal of immunology.

[141]  S. Amara,et al.  Calcitonin/calcitonin gene-related peptide transcription unit: tissue-specific expression involves selective use of alternative polyadenylation sites , 1984, Molecular and cellular biology.

[142]  E. Goetzl,et al.  Inhibition by somatostatin of the proliferation of T-lymphocytes and Molt-4 lymphoblasts. , 1984, Cellular immunology.

[143]  J. Levine,et al.  Modulation of immunity and hypersensitivity by sensory neuropeptides. , 1984, Journal of immunology.

[144]  M. Reinecke,et al.  Immunohistochemical localization of vasoactive intestinal polypeptide (VIP) in Merkel cells of various mammals: evidence for a neuromodulator function of the Merkel cell. , 1983, The Journal of investigative dermatology.

[145]  H. Okamoto,et al.  Human preprovasoactive intestinal polypeptide contains a novel PHI-27-like peptide, PHM-27 , 1983, Nature.

[146]  P. Anand,et al.  Topical capsaicin pretreatment inhibits axon reflex vasodilatation caused by somatostatin and vasoactive intestinal polypeptide in human skin , 1983, British journal of pharmacology.

[147]  B. Seegal,et al.  Angiotensin-converting enzyme: vascular endothelial localization. , 1976, Science.

[148]  V. Kolb-Bachofen,et al.  Nitric oxide in human skin: current status and future prospects. , 1998, The Journal of investigative dermatology.

[149]  R. Granstein,et al.  Calcitonin gene-related peptide and Langerhans cell function. , 1997, The journal of investigative dermatology. Symposium proceedings.

[150]  C. Sternini,et al.  Organization of the peripheral nervous system: autonomic and sensory ganglia. , 1997, The journal of investigative dermatology. Symposium proceedings.

[151]  T. Luger,et al.  The Role of α-Melanocyte-Stimulating Hormone in Cutaneous Biology , 1997 .

[152]  J. M. Lipton,et al.  Anti-inflammatory actions of the neuroimmunomodulator alpha-MSH. , 1997, Immunology today.

[153]  R. Quirion,et al.  A potent and selective CGRP2 agonist, [Cys(Et)2,7]hCGRP alpha: comparison in prototypical CGRP1 and CGRP2 in vitro bioassays. , 1997, Canadian journal of physiology and pharmacology.

[154]  G. Trinchieri,et al.  Calcitonin gene-related peptide inhibits proliferation and antigen presentation by human peripheral blood mononuclear cells: effects on B7, interleukin 10, and interleukin 12. , 1997, The Journal of investigative dermatology.

[155]  D. I. Våge,et al.  The melanocortin receptors: agonists, antagonists, and the hormonal control of pigmentation. , 1996, Recent progress in hormone research.

[156]  S. Lawson.  Chapter 22. Peptides and cutaneous polymodal nociceptor neurones , 1996 .

[157]  B. Gilchrest,et al.  Proopiomelanocortin, its derived peptides, and the skin. , 1996, The Journal of investigative dermatology.

[158]  D. Pozo,et al.  Functional and molecular characterization of VIP receptors and signal transduction in human and rodent immune systems. , 1996, Advances in neuroimmunology.

[159]  S. Lawson.  Peptides and cutaneous polymodal nociceptor neurones. , 1996, Progress in brain research.

[160]  J. Y. Lee,et al.  Pharmacological coupling and functional role for CGRP receptors in the vasodilation of rat pial arterioles. , 1996, The American journal of physiology.

[161]  M. Hilliges,et al.  Ultrastructural evidence for nerve fibers within all vital layers of the human epidermis. , 1995, Journal of Investigative Dermatology.

[162]  L. Misery,et al.  Expression of somatostatin on Langerhans cells. , 1995, Advances in experimental medicine and biology.

[163]  John Brown,et al.  Neuropeptide induction of human microvascular endothelial cell interleukin 8. , 1995 .

[164]  M. Fournié-Zaluski,et al.  Inhibitors of neprilysin: design, pharmacological and clinical applications. , 1995, Methods in enzymology.

[165]  D. Hoyer,et al.  Characterization of somatostatin receptor subtypes. , 1995, Ciba Foundation symposium.

[166]  U. Scapagnini,et al.  Effects of CGRP in different models of mouse ear inflammation. , 1994, Life sciences.

[167]  H. Granger,et al.  Substance P increases cyclic GMP levels on coronary postcapillary venular endothelial cells. , 1993, Life sciences.

[168]  A. Johnson,et al.  Cytokines increase neutral endopeptidase activity in lung fibroblasts. , 1993, American journal of respiratory cell and molecular biology.

[169]  J. Marchand,et al.  Selective in situ hybridization histochemical analyses of alternatively spliced mRNAs encoding β- and γ-preprotachykinins in rat central nervous system , 1993 .

[170]  J. Marchand,et al.  Selective in situ hybridization histochemical analyses of alternatively spliced mRNAs encoding beta- and gamma-preprotachykinins in rat central nervous system. , 1993, Brain research. Molecular brain research.

[171]  P. Benjamin,et al.  Chapter 9 Alternative mRNA splicing in the nervous system , 1992 .

[172]  P. Benjamin,et al.  Alternative mRNA splicing in the nervous system. , 1992, Progress in brain research.

[173]  Y. Okayama,et al.  Mediator secretion from human skin mast cells provoked by immunological and non-immunological stimulation. , 1991, Skin pharmacology : the official journal of the Skin Pharmacology Society.

[174]  J. Streilein,et al.  Tumor necrosis factor-alpha and ultraviolet B light have similar effects on contact hypersensitivity in mice. , 1990, Regional immunology.

[175]  J. Nadel,et al.  Recombinant neutral endopeptidase attenuates substance P-induced plasma extravasation in the guinea pig skin. , 1990, International archives of allergy and applied immunology.

[176]  J. Guilhou.  Growth hormone, somatostatin and psoriasis. , 1990, Dermatologica.

[177]  J. Mcghee,et al.  Expression of substance P and somatostatin receptors on a T helper cell line. , 1987, Advances in experimental medicine and biology.

[178]  O. Johansson.  Evidence for PHI-immunoreactive nerve fibres in the human skin: coexistence with VIP? , 1986, Medical biology.

[179]  O. Johansson.  A detailed account of NPY-immunoreactive nerves and cells of the human skin. Comparison with VIP-, substance P- and PHI-containing structures. , 1986, Acta physiologica Scandinavica.

[180]  M. Blaustein.  Intracellular Calcium as a Second Messenger , 1985 .

[181]  S. Reichlin.  Somatostatin (First of two parts) , 1983 .

[182]  G. Dockray.  Evolutionary relationships of the gut hormones. , 1979, Federation proceedings.

[183]  H. Zachariae,et al.  Histamine and plasma kinins in delayed allergic skin reactions. , 1970, Allergie und Asthma.