Journal of Neuroimmunology
Volume 221, Issue 1 , Pages 62-67 , 15 April 2010

Midregional Proenkephalin A and N-terminal Protachykinin A are decreased in the cerebrospinal fluid of patients with dementia disorders and acute neuroinflammation

  • Andrea Ernst

      Affiliations

    • Research Department, B.R.A.H.M.S. AG, Biotechnology Centre Hennigsdorf/Berlin, Germany
    • SphingoTec GmbH, Borgsdorf, Germany
    • Institut für Experimentelle Endokrinologie & EnForCé, Charité-Universitätsmedizin Berlin, Germany
    • Corresponding Author InformationCorresponding author. Research Department, B.R.A.H.M.S AG, Biotechnology Centre, Neuendorfstr. 25, D-16761 Hennigsdorf, Germany. Tel.: +49 3302 883685; fax: +49 3302 883621.
  • ,
  • Katharina Buerger

      Affiliations

    • Department of Psychiatry, Alzheimer Memorial Center, Ludwig-Maximilian University, Munich, Germany
  • ,
  • Oliver Hartmann

      Affiliations

    • Research Department, B.R.A.H.M.S. AG, Biotechnology Centre Hennigsdorf/Berlin, Germany
  • ,
  • Richard Dodel

      Affiliations

    • Department of Neurology, Philipps-University Marburg, Marburg, Germany
  • ,
  • Carmen Noelker

      Affiliations

    • Department of Neurology, Philipps-University Marburg, Marburg, Germany
  • ,
  • Norbert Sommer

      Affiliations

    • Department of Neurology, Philipps-University Marburg, Marburg, Germany
  • ,
  • Markus Schwarz

      Affiliations

    • Department of Psychiatry, Alzheimer Memorial Center, Ludwig-Maximilian University, Munich, Germany
  • ,
  • Josef Köhrle

      Affiliations

    • Institut für Experimentelle Endokrinologie & EnForCé, Charité-Universitätsmedizin Berlin, Germany
  • ,
  • Andreas Bergmann

      Affiliations

    • Research Department, B.R.A.H.M.S. AG, Biotechnology Centre Hennigsdorf/Berlin, Germany
    • SphingoTec GmbH, Borgsdorf, Germany
  • ,
  • Harald Hampel

      Affiliations

    • Department of Psychiatry, Alzheimer Memorial Center, Ludwig-Maximilian University, Munich, Germany
    • Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience (TCIN), Trinity College Dublin, Trinity Centre for Health Sciences, The Adelaide and Meath Hospital Incorporating The National Children's Hospital (AMiNHC), Dublin, Ireland

Received 1 December 2009 ,Revised 3 February 2010 ,Accepted 3 February 2010.

References 

  1. Aebi C, Monsch AU, Berres M, Brubacher D, Staehelin HB, GC-NS G. Validation of the German CERAD-neuropsychological assessment battery. Neurobiol. Aging. 2002;23:S27
  2. Aimone LD, Yaksh TL. Opioid modulation of capsaicin-evoked release of substance P from rat spinal cord in vivo. Peptides. 1989;10:1127–1131
  3. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al. Inflammation and Alzheimer's disease. Neurobiol. Aging. 2000;21:383–421
  4. Almay BG, Johansson F, von Knorring L, Sakurada T, Terenius L. Long-term high frequency transcutaneous electrical nerve stimulation (hi-TNS) in chronic pain. Clinical response and effects on CSF-endorphins, monoamine metabolites, substance P-like immunoreactivity (SPLI) and pain measures. J Psychosom Res. 1985;29:247–257
  5. Blennow K, Hampel H. CSF markers for incipient Alzheimer's disease. Lancet Neurol. 2003;2:605–613
  6. Bonifati DM, Kishore U. Role of complement in neurodegeneration and neuroinflammation. Mol. Immunol. 2007;44:999–1010
  7. Bosco DA, Fowler DM, Zhang Q, Nieva J, Powers ET, Wentworth P, et al. Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fibrilization. Nat Chem Biol. 2006;2:249–253
  8. Carrillo MC, Blackwell A, Hampel H, Lindborg J, Sperling R, Schenk D, et al. Early risk assessment for Alzheimer's disease. Alzheimers Dement. 2009;5:182–196
  9. Chretien M, Seidah NG. Chemistry and biosynthesis of pro-opiomelanocortin. ACTH, MSH's, endorphins and their related peptides. Mol. Cell. Biochem. 1981;34:101–127
  10. Ciesla A, Pierzchala-Koziec K, Mach T, Garlicki A, Bociaga-Jasik M. Met-enkephalin in the cerebrospinal fluid as an indicator of central nervous system injury in meningitis and encephalitis. Pol Merkur Lekarski. 2005;18:549–551
  11. Comb M, Seeburg PH, Adelman J, Eiden L, Herbert E. Primary structure of the human Met- and Leu-enkephalin precursor and its mRNA. Nature. 1982;295:663–666
  12. Conlon JM, Sheehan L. Conversion of substance P to C-terminal fragments in human plasma. Regul. Pept. 1983;7:335–345
  13. Cramer H, Schaudt D, Rissler K, Strubel D, Warter JM, Kuntzmann F. Somatostatin-like immunoreactivity and substance-P-like immunoreactivity in the CSF of patients with senile dementia of Alzheimer type, multi-infarct syndrome and communicating hydrocephalus. J Neurol. 1985;232:346–351
  14. Denning GM, Ackermann LW, Barna TJ, Armstrong JG, Stoll LL, Weintraub NL, et al. Proenkephalin expression and enkephalin release are widely observed in non-neuronal tissues. Peptides. 2008;29:83–92
  15. Engelhart MJ, Geerlings MI, Meijer J, Kiliaan A, Ruitenberg A, van Swieten JC, et al. Inflammatory proteins in plasma and the risk of dementia: the Rotterdam study. Arch. Neurol. 2004;61:668–672
  16. Ernst A, Kohrle J, Bergmann A. Proenkephalin A 119–159, a stable proenkephalin A precursor fragment identified in human circulation. Peptides. 2006;27:1835–1840
  17. Ernst A, Morgenthaler NG, Buerger K, Dodel R, Noelker C, Sommer N, et al. Procalcitonin is elevated in the cerebrospinal fluid of patients with dementia and acute neuroinflammation. J Neuroimmunol. 2007;189:169–174
  18. Ernst A, Suhr J, Kohrle J, Bergmann A. Detection of stable N-terminal protachykinin A immunoreactivity in human plasma and cerebrospinal fluid. Peptides. 2008;29:1201–1206
  19. Ewers M, Zhong Z, Burger K, Wallin A, Blennow K, Teipel SJ, et al. Increased CSF-BACE 1 activity is associated with ApoE-epsilon 4 genotype in subjects with mild cognitive impairment and Alzheimer's disease. Brain. 2008;131:1252–1258
  20. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975;12:189–198
  21. Gupta A, Pansari K. Inflammation and Alzheimer's disease. Int. J. Clin. Pract. 2003;57:36–39
  22. Gupta A, Watkins A, Thomas P, Majer R, Habubi N, Morris G, et al. Coagulation and inflammatory markers in Alzheimer's and vascular dementia. Int. J. Clin. Pract. 2005;59:52–57
  23. Hampel H, Broich K. Enrichment of MCI and early Alzheimer's disease Treatment trials using neurochemical and imaging candidate biomarkers. J Nutr Health Aging. 2009;13:373–375
  24. Hampel H, Buerger K, Zinkowski R, Teipel SJ, Goernitz A, Andreasen N, et al. Measurement of phosphorylated tau epitopes in the differential diagnosis of Alzheimer disease: a comparative cerebrospinal fluid study. Arch. Gen. Psychiatry. 2004;61:95–102
  25. Hampel H, Burger K, Teipel SJ, Bokde AL, Zetterberg H, Blennow K. Core candidate neurochemical and imaging biomarkers of Alzheimer's disease. Alzheimers Dement. 2008;4:38–48
  26. Han JS, Chen XH, Sun SL, Xu XJ, Yuan Y, Yan SC, et al. Effect of low- and high-frequency TENS on Met-enkephalin-Arg-Phe and dynorphin A immunoreactivity in human lumbar CSF. Pain. 1991;47:295–298
  27. Harrison S, Geppetti P. Substance p. Int. J. Biochem. Cell Biol. 2001;33:555–576
  28. Hasenohrl RU, Souza-Silva MA, Nikolaus S, Tomaz C, Brandao ML, Schwarting RK, et al. Substance P and its role in neural mechanisms governing learning, anxiety and functional recovery. Neuropeptides. 2000;34:272–280
  29. Ho WZ, Lai JP, Zhu XH, Uvaydova M, Douglas SD. Human monocytes and macrophages express substance P and neurokinin-1 receptor. J Immunol. 1997;159:5654–5660
  30. Horikawa S, Takai T, Toyosato M, Takahashi H, Noda M, Kakidani H, et al Isolation and structural organization of the human preproenkephalin B gene. Nature. 1983;306:611–614
  31. Jia JP, Meng R, Sun YX, Sun WJ, Ji XM, Jia LF. Cerebrospinal fluid tau, Abeta1-42 and inflammatory cytokines in patients with Alzheimer's disease and vascular dementia. Neurosci. Lett. 2005;383:12–16
  32. Katsuse O, Iseki E, Kosaka K. Immunohistochemical study of the expression of cytokines and nitric oxide synthases in brains of patients with dementia with Lewy bodies. Neuropathology. 2003;23:9–15
  33. Korshunova TS, Kolii GA, Larskii EG, Ivanova-Smolenskaia IA, Markova ED. Endogenous morphines in chronic progressive diseases of the central nervous system. Zh. Nevropatol. Psikhiatr. Im. S. S. Korsakova. 1984;84:1061–1064
  34. Lai JP, Douglas SD, Ho WZ. Human lymphocytes express substance P and its receptor. J Neuroimmunol. 1998;86:80–86
  35. Mackenzie IR. Activated microglia in dementia with Lewy bodies. Neurology. 2000;55:132–134
  36. Mackenzie IR. Cortical inflammation in dementia with Lewy bodies. Arch. Neurol. 2001;58:519–520
  37. Martinez M, Frank A, Hernanz A. Relationship of interleukin-1 beta and beta 2-microglobulin with neuropeptides in cerebrospinal fluid of patients with dementia of the Alzheimer type. J Neuroimmunol. 1993;48:235–240
  38. McKeith IG, Galasko D, Kosaka K, Perry EK, Dickson DW, Hansen LA, et al. Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): report of the consortium on DLB international workshop. Neurology. 1996;47:1113–1124
  39. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. 1984;34:939–944
  40. Mosnaim AD, Puente J, Wolf ME, Callaghan OH, Busch R, Diamond S. Studies of the in vitro human plasma degradation of methionine-enkephalin. Gen. Pharmacol. 1988;19:729–733
  41. Muhlbauer M, Metcalf JC, Robertson JT, Fridland G, Desiderio DM. Opioid peptides in the cerebrospinal fluid of Alzheimer patients. Biomed. Chromatogr. 1986;1:155–158
  42. Nawa H, Kotani H, Nakanishi S. Tissue-specific generation of two preprotachykinin mRNAs from one gene by alternative RNA splicing. Nature. 1984;312:729–734
  43. Nyberg F. Opioid peptides in cerebrospinal fluid-methods for analysis and their significance in the clinical perspective. Front Biosci. 2004;9:3510–3525
  44. Pittius CW, Seizinger BR, Mehraein P, Pasi A, Herz A. Proenkephalin-A-derived peptides are present in human brain. Life Sci. 1983;33(Suppl 1):41–44
  45. Plotnikoff NP, Faith RE, Murgo AJ, Herberman RB, Good RA. Methionine enkephalin: a new cytokine–human studies. Clin. Immunol. Immunopathol. 1997;82:93–101
  46. Przewlocki R, Przewlocka B. Opioids in chronic pain. Eur. J. Pharmacol. 2001;429:79–91
  47. Qureshi GA, Baig SM, Parvez SH. Variation in cerebrospinal fluid levels of neuropeptide Y, cholecystokinin and substance P in patients with neurological disorders. Neuroendocrinol Lett. 2000;21:409–416
  48. Rentzos M, Zoga M, Paraskevas GP, Kapaki E, Rombos A, Nikolaou C, et al. IL-15 is elevated in cerebrospinal fluid of patients with Alzheimer's disease and frontotemporal dementia. J Geriatr Psychiatry Neurol. 2006;19:114–117
  49. Roman GC, Tatemichi TK, Erkinjuntti T, Cummings JL, Masdeu JC, Garcia JH, et al Vascular dementia: diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurology. 1993;43:250–260
  50. Rosler N, Wichart I, Jellinger KA. Ex vivo lumbar and post mortem ventricular cerebrospinal fluid substance P-immunoreactivity in Alzheimer's disease patients. Neurosci. Lett. 2001;299:117–120
  51. Samuelsson H, Ekman R, Hedner T. CSF neuropeptides in cancer pain: effects of spinal opioid therapy. Acta Anaesthesiol. Scand. 1993;37:502–508
  52. Schmidt KH, Metzler P. Wortschatztest (WST). Beltz Test GmbH: Weinheim; 1992;
  53. Schulteis G, Martinez JL. Peripheral modulation of learning and memory: enkephalins as a model system. Psychopharmacology (Berl). 1992;109:347–364
  54. Senba E, Yanaihara C, Yanaihara N, Tohyama M. Co-localization of substance P and Met-enkephalin-Arg6-Gly7-Leu8 in the intraspinal neurons of the rat, with special reference to the neurons in the substantia gelatinosa. Brain Res. 1988;453:110–116
  55. Severini C, Improta G, Falconieri-Erspamer G, Salvadori S, Erspamer V. The tachykinin peptide family. Pharmacol. Rev. 2002;54:285–322
  56. Sjogren M, Folkesson S, Blennow K, Tarkowski E. Increased intrathecal inflammatory activity in frontotemporal dementia: pathophysiological implications. J Neurol Neurosurg Psychiatry. 2004;75:1107–1111
  57. Sulkava R, Erkinjuntti T, Laatikainen T. CSF beta-endorphin and beta-lipotropin in Alzheimer's disease and multi-infarct dementia. Neurology. 1985;35:1057–1058
  58. Sunderland T, Berrettini WH, Molchan SE, Lawlor BA, Martinez RA, Vitiello B, et al. Reduced cerebrospinal fluid dynorphin A1-8 in Alzheimer's disease. Biol. Psychiatry. 1991;30:81–87
  59. The Lund and Manchester Groups . Clinical and neuropathological criteria for frontotemporal dementia. J. Neurol. Neurosurg. Psychiatry. 1994;57:416–418
  60. Wada-Isoe K, Wakutani Y, Urakami K, Nakashima K. Elevated interleukin-6 levels in cerebrospinal fluid of vascular dementia patients. Acta Neurol. Scand. 2004;110:124–127
  61. Zhong Z, Ewers M, Teipel S, Burger K, Wallin A, Blennow K, et al. Levels of beta-secretase (BACE1) in cerebrospinal fluid as a predictor of risk in mild cognitive impairment. Arch. Gen. Psychiatry. 2007;64:718–726
  62. Zubrzycka M, Janecka A. Substance P: transmitter of nociception (Mini review). Endocr. Regul. 2000;34:195–201

PII: S0165-5728(10)00049-4

doi: 10.1016/j.jneuroim.2010.02.004

Journal of Neuroimmunology
Volume 221, Issue 1 , Pages 62-67 , 15 April 2010