Upregulation of nuclear factor-kappaB expression by SLURP-1 is mediated by alpha7-nicotinic acetylcholine receptor and involves both ionic events and activation of protein kinases.

SLURP-1 (secreted mammalian Ly-6/urokinase plasminogen activator receptor-related protein-1) is a novel auto/paracrine cholinergic peptide that can bind to α(7)-nicotinic acetylcholine receptor (nAChR), a high Ca(2+)-permeable ion channel coupled to regulation of nuclear factor-κB (NF-κB) expression. Elucidation of intracellular signaling events elicited by SLURP-1 is crucial for understanding the molecular mechanism of functioning of this novel hormone-like peptide that alters vital cell functions and can protect from tumorigenic transformation. In this study, we sought to dissect out the role of α(7)-nAChR in mediating the biologic effects of recombinant SLURP-1 on the immortalized line of human oral keratinocytes Het-1A. A multifold upregulation of the NF-κB expression at the mRNA and protein levels by SLURP-1 was only slightly diminished due to elimination of Na(+), whereas in Ca(2+)-free medium the effect of SLURP-1 was inhibited by >50%. Both in the absence of extracellular Ca(2+) and in the presence of Cd(2+) or Zn(2+), the SLURP-1-dependent elevation of NF-κB was almost completely blocked by inhibiting MEK1 activity. Downstream of α(7)-nAChR, the SLURP-1 signaling coupled to upregulation of NF-κB also involved Jak2 as well as Ca(2+)/calmodulin-dependent kinase II (CaMKII) and protein kinase C (PKC), whose inhibition significantly (P < 0.05) reduced the SLURP-1-induced upregulation of NF-κB. The obtained results indicated that activation of α(7)-nAChR by SLURP-1 leads to upregulation of the NF-κB gene expression due to activation of the Raf-1/MEK1/ERK1/2 cascade that proceeds via two complementary signaling pathways. One is mediated by the Ca(2+)-entry dependent CaMKII/PKC activation and another one by Ca(2+)-independent involvement of Jak2. Thus, there exists a previously not appreciated network of noncanonical auto/paracrine ligands of nAChR of the Ly-6 protein family, which merits further investigations.

[1]  J. Wityak,et al.  Beyond U0126. Dianion chemistry leading to the rapid synthesis of a series of potent MEK inhibitors. , 2004, Bioorganic & medicinal chemistry letters.

[2]  Laure Plantard,et al.  Identification of SLURP-1 as an epidermal neuromodulator explains the clinical phenotype of Mal de Meleda. , 2003, Human molecular genetics.

[3]  P. Granone,et al.  α7-Nicotinic Acetylcholine Receptors Affect Growth Regulation of Human Mesothelioma Cells , 2004, Cancer Research.

[4]  R. Miledi,et al.  Effects of Zn2+ on wild and mutant neuronal α7 nicotinic receptors , 1998 .

[5]  C. Southan,et al.  The characterisation of novel secreted Ly‐6 proteins from rat urine by the combined use of two‐dimensional gel electrophoresis, microbore high performance liquid chromatography and expressed sequence tag data , 2002, Proteomics.

[6]  T. X. Lee,et al.  Activation of keratinocyte nicotinic cholinergic receptors stimulates calcium influx and enhances cell differentiation. , 1996, The Journal of investigative dermatology.

[7]  S. Grando Basic and clinical aspects of non-neuronal acetylcholine: biological and clinical significance of non-canonical ligands of epithelial nicotinic acetylcholine receptors. , 2008, Journal of pharmacological sciences.

[8]  A. Khorram-Manesh,et al.  Nicotine induced modulation of SLURP-1 expression in human colon cancer cells , 2009, Autonomic Neuroscience.

[9]  T. Malek,et al.  Characterization of two novel Ly-6 genes. Protein sequence and potential structural similarity to alpha-bungarotoxin and other neurotoxins. , 1993, Journal of immunology.

[10]  H. Inoko,et al.  SLURP-2, a novel member of the human Ly-6 superfamily that is up-regulated in psoriasis vulgaris. , 2003, Genomics.

[11]  R. Buchli,et al.  Choline Acetyltransferase, Acetylcholinesterase, and Nicotinic Acetylcholine Receptors of Human Gingival and Esophageal Epithelia , 2000, Journal of dental research.

[12]  M. Pittelkow,et al.  Adrenergic and cholinergic control in the biology of epidermis: physiological and clinical significance. , 2006, The Journal of investigative dermatology.

[13]  S. Grando,et al.  SLURP‐2: A novel cholinergic signaling peptide in human mucocutaneous epithelium , 2006, Journal of cellular physiology.

[14]  M. Chabbert,et al.  Identification of lynx2, a novel member of the ly-6/neurotoxin superfamily, expressed in neuronal subpopulations during mouse development , 2006, Molecular and Cellular Neuroscience.

[15]  C. Kirkpatrick,et al.  Acetylcholine beyond neurons: the non‐neuronal cholinergic system in humans , 2008, British journal of pharmacology.

[16]  D. Bercovich,et al.  Functional role of alpha7 nicotinic receptor in physiological control of cutaneous homeostasis. , 2003, Life sciences.

[17]  S. Grando,et al.  Biological effects of SLURP-1 on human keratinocytes. , 2005, The Journal of investigative dermatology.

[18]  T. Himi,et al.  Expression of SLURP‐1, an endogenous α7 nicotinic acetylcholine receptor allosteric ligand, in murine bronchial epithelial cells , 2009, Journal of neuroscience research.

[19]  S. Waguri,et al.  Primary sensory neuronal expression of SLURP-1, an endogenous nicotinic acetylcholine receptor ligand , 2009, Neuroscience Research.

[20]  M. Runge,et al.  Thrombin Regulates Vascular Smooth Muscle Cell Growth and Heat Shock Proteins via the JAK-STAT Pathway* , 2001, The Journal of Biological Chemistry.

[21]  D. Bercovich,et al.  Central role of α7 nicotinic receptor in differentiation of the stratified squamous epithelium , 2002, The Journal of Cell Biology.

[22]  S. Grando,et al.  Novel human alpha9 acetylcholine receptor regulating keratinocyte adhesion is targeted by Pemphigus vulgaris autoimmunity. , 2000, The American journal of pathology.

[23]  S. Grando,et al.  The nicotinic receptor antagonists abolish pathobiologic effects of tobacco-derived nitrosamines on BEP2D cells , 2006, Journal of Cancer Research and Clinical Oncology.

[24]  S. Grando,et al.  The Ras/Raf-1/MEK1/ERK Signaling Pathway Coupled to Integrin Expression Mediates Cholinergic Regulation of Keratinocyte Directional Migration* , 2005, Journal of Biological Chemistry.

[25]  A. Beaudet,et al.  Receptor-mediated tobacco toxicity: regulation of gene expression through alpha3beta2 nicotinic receptor in oral epithelial cells. , 2005, The American journal of pathology.

[26]  L. Marubio,et al.  Differential regulation of keratinocyte chemokinesis and chemotaxis through distinct nicotinic receptor subtypes , 2004, Journal of Cell Science.

[27]  J. Piatigorsky,et al.  Postnatal gene expression in the normal mouse cornea by SAGE. , 2004, Investigative ophthalmology & visual science.

[28]  Jen-kun Lin,et al.  Tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) induces cell proliferation in normal human bronchial epithelial cells through NFκB activation and cyclin D1 up-regulation , 2005 .

[29]  K. Kawashima,et al.  Immune system expression of SLURP-1 and SLURP-2, two endogenous nicotinic acetylcholine receptor ligands. , 2007, Life sciences.

[30]  K. Pinkerton,et al.  Receptor-mediated tobacco toxicity: alterations of the NF-kappaB expression and activity downstream of alpha7 nicotinic receptor in oral keratinocytes. , 2007, Life sciences.

[31]  C. Metz,et al.  Nicotine Inhibits Cytokine Production by Placenta Cells via NFκB: Potential Role in Pregnancy-Induced Hypertension , 2007, Molecular medicine.

[32]  Robert G. Parton,et al.  GTP-dependent segregation of H-ras from lipid rafts is required for biological activity , 2001, Nature Cell Biology.

[33]  S. Manna,et al.  Long term environmental tobacco smoke activates nuclear transcription factor-kappa B, activator protein-1, and stress responsive kinases in mouse brain. , 2006, Biochemical pharmacology.

[34]  A. Tekinay,et al.  Prostate Stem Cell Antigen Is an Endogenous lynx1-Like Prototoxin That Antagonizes α7-Containing Nicotinic Receptors and Prevents Programmed Cell Death of Parasympathetic Neurons , 2009, The Journal of Neuroscience.

[35]  Ana Canda-Sánchez,et al.  IL-12-dependent activation of ERK1/2 in human T lymphoblasts. , 2009, Immunobiology.

[36]  A. Sali,et al.  lynx1, an Endogenous Toxin-like Modulator of Nicotinic Acetylcholine Receptors in the Mammalian CNS , 1999, Neuron.

[37]  S. Grando,et al.  Cholinergic control of epidermal cohesion , 2006, Experimental dermatology.

[38]  J. Sullivan,et al.  Activation of the recombinant human alpha 7 nicotinic acetylcholine receptor significantly raises intracellular free calcium. , 1997, The Journal of pharmacology and experimental therapeutics.

[39]  E. Albuquerque,et al.  alpha-Bungarotoxin-sensitive hippocampal nicotinic receptor channel has a high calcium permeability. , 1995, Biophysical journal.

[40]  David John Adams,et al.  Monovalent and divalent cation permeability and block of neuronal nicotinic receptor channels in rat parasympathetic ganglia , 1995, The Journal of general physiology.

[41]  S. K. Kang,et al.  Interleukin‐6 induces proliferation in adult spinal cord‐derived neural progenitors via the JAK2/STAT3 pathway with EGF‐induced MAPK phosphorylation , 2008, Cell proliferation.

[42]  D L Simmons,et al.  CD59, an LY-6-like protein expressed in human lymphoid cells, regulates the action of the complement membrane attack complex on homologous cells , 1989, The Journal of experimental medicine.

[43]  R. Sorenson,et al.  Prolactin receptors and JAK2 in islets of Langerhans: an immunohistochemical analysis. , 1995, Endocrinology.

[44]  J. Gills,et al.  Tobacco components stimulate Akt-dependent proliferation and NFkappaB-dependent survival in lung cancer cells. , 2005, Carcinogenesis.

[45]  F. Tamanoi,et al.  Identification of Ras farnesyltransferase inhibitors by microbial screening. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. A. Harris,et al.  The discovery of potent cRaf1 kinase inhibitors. , 2000, Bioorganic & medicinal chemistry letters.

[47]  J. Weissenbach,et al.  Mutations in the gene encoding SLURP-1 in Mal de Meleda. , 2001, Human molecular genetics.

[48]  Koichi Ito,et al.  Nicotine inhibits the production of inflammatory mediators in U937 cells through modulation of nuclear factor-kappaB activation. , 1998, Biochemical and biophysical research communications.

[49]  J. Patrick,et al.  Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  D. Hohl,et al.  SLURP1 is a late marker of epidermal differentiation and is absent in Mal de Meleda. , 2007, The Journal of investigative dermatology.

[51]  S. Wattler,et al.  Structural and phylogenetic characterization of human SLURP‐1, the first secreted mammalian member of the Ly‐6/uPAR protein superfamily , 2008, Protein science : a publication of the Protein Society.

[52]  M L van Hoek,et al.  Phosphotyrosine phosphatase activity associated with c-Src in large multimeric complexes isolated from adrenal medullary chromaffin cells. , 1997, The Biochemical journal.

[53]  E. Albuquerque,et al.  A nicotinic acetylcholine receptor regulating cell adhesion and motility is expressed in human keratinocytes. , 1995, The Journal of investigative dermatology.

[54]  Yasushi Matsumura,et al.  Involvement of Nuclear Factor-&kgr;B and Apoptosis Signal-Regulating Kinase 1 in G-Protein–Coupled Receptor Agonist–Induced Cardiomyocyte Hypertrophy , 2002, Circulation.

[55]  C. Gotti,et al.  Neuronal nicotinic receptors: from structure to pathology , 2004, Progress in Neurobiology.

[56]  J. Qian,et al.  Coupling of ionic events to protein kinase signaling cascades upon activation of alpha7 nicotinic receptor: cooperative regulation of alpha2-integrin expression and Rho kinase activity. , 2009, The Journal of biological chemistry.

[57]  A. Leonardi,et al.  Nicotine induces tissue factor expression in cultured endothelial and smooth muscle cells , 2006, Journal of thrombosis and haemostasis : JTH.

[58]  N. Heintz,et al.  Novel Modulation of Neuronal Nicotinic Acetylcholine Receptors by Association with the Endogenous Prototoxin lynx1 , 2002, Neuron.

[59]  S. Fucile Ca2+ permeability of nicotinic acetylcholine receptors. , 2004, Cell calcium.

[60]  W. Wu,et al.  The Modulating Role of Nuclear Factor-κB in the Action of α7-Nicotinic Acetylcholine Receptor and Cross-Talk between 5-Lipoxygenase and Cyclooxygenase-2 in Colon Cancer Growth Induced by 4-(N-Methyl-N-nitrosamino)-1-(3-pyridyl)-1-butanone , 2004, Journal of Pharmacology and Experimental Therapeutics.

[61]  M. Biffoni,et al.  ARS Component B: structural characterization, tissue expression and regulation of the gene and protein (SLURP-1) associated with Mal de Meleda. , 2003, European journal of dermatology : EJD.

[62]  D. Rifkin,et al.  Cellular glycosylphosphatidylinositol‐specific phospholipase D regulates urokinase receptor shedding and cell surface expression , 1999, Journal of cellular physiology.

[63]  Seungho Wang,et al.  Signaling pathways of magnolol‐induced adrenal steroidogensis , 2005, FEBS letters.

[64]  A. Khorram-Manesh,et al.  Expression of the endogenous, nicotinic acetylcholine receptor ligand, SLURP-1, in human colon cancer. , 2008, Autonomic & autacoid pharmacology.

[65]  T. Matsumiya,et al.  Production of growth related oncogene protein-alpha in human umbilical vein endothelial cells stimulated with soluble interleukin-6 receptor-alpha: role of signal transducers, janus kinase 2 and mitogen-activated kinase kinase. , 2002, Life sciences.

[66]  N. Sitaram,et al.  Seminalplasmin and caltrin are the same protein , 1986, FEBS letters.

[67]  J. Macor,et al.  A chiral synthesis of (-)-spiro[1-azabicyclo[2.2.2]octane-3,5'- oxazolidin-2'-one]: a conformationally restricted analogue of acetylcholine that is a potent and selective alpha7 nicotinic receptor agonist. , 2004, The Journal of organic chemistry.

[68]  J. Steinbach,et al.  Mechanism of action of the nicotinic acetylcholine receptor. , 2007, Ciba Foundation symposium.

[69]  K. Pinkerton,et al.  Receptor‐mediated tobacco toxicity: cooperation of the Ras/Raf‐1/MEK1/ERK and JAK‐2/STAT‐3 pathways downstream of a7 nicotinic receptor in oral keratinocytes , 2006 .

[70]  D. Vetter,et al.  Central role of alpha9 acetylcholine receptor in coordinating keratinocyte adhesion and motility at the initiation of epithelialization. , 2007, Experimental cell research.

[71]  R. Macleod,et al.  Studies on an antineoplastic fraction from human urine. Characterization of the major protein in this fraction. , 1986, The Biochemical journal.

[72]  Qiang Liu,et al.  Dissecting the signaling pathway of nicotine‐mediated neuroprotection in a mouse Alzheimer disease model , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[73]  S. Grando,et al.  Overexpression of SLURP-1 and -2 alleviates the tumorigenic action of tobacco-derived nitrosamine on immortalized oral epithelial cells. , 2007, Biochemical pharmacology.

[74]  J. Ooi,et al.  A novel molecule, SLURP-1, enhances the survival of periodontal ligament fibroblasts. , 2010, Journal of periodontal research.

[75]  D. Bertrand,et al.  A Novel Human Nicotinic Receptor Subunit, α10, That Confers Functionality to the α9-Subunit , 2002 .

[76]  S. Grando,et al.  Nicotinic receptors mediate tumorigenic action of tobacco-derived nitrosamines on immortalized oral epithelial cells , 2006, Cancer biology & therapy.

[77]  R. Palfree Ly-6-domain proteins--new insights and new members: a C-terminal Ly-6 domain in sperm acrosomal protein SP-10. , 1996, Tissue antigens.

[78]  K. Okutomi,et al.  Isolation and characterization of a new member of the human Ly6 gene family (LY6H). , 1998, Genomics.

[79]  S. Grando,et al.  SLURP-1 and -2 in normal, immortalized and malignant oral keratinocytes. , 2007, Life sciences.

[80]  C. Harris,et al.  Establishment and characterization of SV40 T-antigen immortalized human esophageal epithelial cells. , 1991, Cancer research.

[81]  Lan Li,et al.  Nicotine Induces Proinflammatory Responses in Macrophages and the Aorta Leading to Acceleration of Atherosclerosis in Low-Density Lipoprotein Receptor−/− Mice , 2006, Arteriosclerosis, thrombosis, and vascular biology.

[82]  M. Bencherif,et al.  Convergence of alpha 7 nicotinic acetylcholine receptor-activated pathways for anti-apoptosis and anti-inflammation: Central role for JAK2 activation of STAT3 and NF-κB , 2009, Brain Research.

[83]  K. Pinkerton,et al.  Receptor‐mediated tobacco toxicity: acceleration of sequential expression of α5 and α7 nicotinic receptor subunits in oral keratinocytes exposed to cigarette smoke , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[84]  H. Kurzen,et al.  Phenotypical and molecular profiling of the extraneuronal cholinergic system of the skin. , 2004, The Journal of investigative dermatology.