Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology
Volume 113, Issue 2 , Pages 239-244 , February 2012

Adhesion molecule L1 is down-regulated in malignant peripheral nerve sheath tumors versus benign neurofibromatosis type 1–associated tumors

  • Marco Blessmann, MD, DMD, PhD

      Affiliations

    • Department of Oral and Maxillofacial Surgery, University Medical Center Hamburg-Eppendorf, Germany
    • Corresponding Author InformationReprint requests: Marco Blessmannn, MD, DMD, Department of Oral and Maxillofacial Surgery, University Medical Center Hamburg-Eppendorf, Martinistraße 52, 20246 Hamburg, Germany
  • ,
  • Alexander Gröbe, MD, DMD

      Affiliations

    • Department of Oral and Maxillofacial Surgery, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Alexander Quaas, MD

      Affiliations

    • Institute for Pathology, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Jussuf T. Kaifi, MD, PhD

      Affiliations

    • Department of General, Visceral, and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Georgios Mistakidis, MD, DMD

      Affiliations

    • Department of Oral and Maxillofacial Surgery, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Christian Bernreuther, MD, PhD

      Affiliations

    • Department of Neuropathology, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Guido Sauter, MD, PhD

      Affiliations

    • Institute for Pathology, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Stephanie Gros, MD

      Affiliations

    • Department of General, Visceral, and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Tamina Rawnaq, MD

      Affiliations

    • Department of General, Visceral, and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Reinhard Friedrich, MD, DMD, PhD

      Affiliations

    • Department of Oral and Maxillofacial Surgery, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Victor F. Mautner, MD, PhD

      Affiliations

    • Department of Oral and Maxillofacial Surgery, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Ralf Smeets, MD, DMD, PhD

      Affiliations

    • Department of Oral and Maxillofacial Surgery, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Max Heiland, MD, DMD, PhD

      Affiliations

    • Department of Oral and Maxillofacial Surgery, University Medical Center Hamburg-Eppendorf, Germany
  • ,
  • Melitta Schachner, ScD, PhD

      Affiliations

    • Center for Molecular Neurobiology, University Medical Center Hamburg-Eppendorf, Germany
    • Center for Neuroscience, Shantou University Medical College, Shantou, China
    • Corresponding Author InformationMelitta Schachner, ScD, PhD, Center for Neuroscience, Shantou University Medical College, 22 Xin Ling Road, Shantou 515041, P.R. China
  • ,
  • Jakob R. Izbicki, MD, PhD

      Affiliations

    • Department of General, Visceral, and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Germany

Received 6 January 2011 ,Revised 14 April 2011 ,Accepted 15 April 2011.

References 

  1. Holtkamp N , Mautner VF , Friedrich RE , Harder A , Hartmann C , Theallier-Janko A , et al.  Differentially expressed genes in neurofibromatosis 1–associated neurofibromas and malignant peripheral nerve sheath tumors . Acta Neuropathol . 2004;107:159–168
  2. Lott IT , Richardson EP . Neuropathological findings and the biology of neurofibromatosis . Adv Neurol . 1981;29:23–32
  3. Evans DG , Baser ME , McGaughran J , Sharif S , Howard E , Moran A . Malignant peripheral nerve sheath tumours in neurofibromatosis 1 . J Med Genet . 2002;39:311–314
  4. Rasmussen SA , Yang Q , Friedman JM . Mortality in neurofibromatosis 1: an analysis using U.S. death certificates . Am J Hum Genet . 2001;68:1110–1118
  5. Watanabe T , Oda Y , Tamiya S , Masuda K , Tsuneyoshi M . Malignant peripheral nerve sheath tumour arising within neurofibroma (An immunohistochemical analysis in the comparison between benign and malignant components) . J Clin Pathol . 2001;54:631–636
  6. Zoller ME , Rembeck B , Oden A , Samuelsson M , Angervall L . Malignant and benign tumors in patients with neurofibromatosis type 1 in a defined Swedish population . Cancer . 1997;79:2125–2131
  7. Friedrich RE , Hartmann M , Mautner VF . Malignant peripheral nerve sheath tumors (MPNST) in NF1-affected children . Anticancer Res . 2007;27:1957–1960
  8. Hagel C , Zils U , Peiper M , Kluwe L , Gotthard S , Friedrich RE , et al.  Histopathology and clinical outcome of NF1-associated vs. sporadic malignant peripheral nerve sheath tumors . J Neuro Oncol . 2007;82:187–192
  9. Tonsgard JH . Clinical manifestations and management of neurofibromatosis type 1 . Semin Pediatr Neurol . 2006;13:2–7
  10. Kaifi JT , Zinnkann U , Yekebas EF , Schurr PG , Reichelt U , Wachowiak R , et al.  L1 is a potential marker for poorly differentiated pancreatic neuroendocrine carcinoma . World J Gastroenterol . 2006;12:94–98
  11. Fidler IJ . Critical determinants of metastasis . Semin Cancer Biol . 2002;12:89–96
  12. Ohnishi T , Matsumura H , Izumoto S , Hiraga S , Hayakawa T . A novel model of glioma cell invasion using organotypic brain slice culture . Cancer Res . 1998;58:2935–2940
  13. Schachner M . Neural recognition molecules and synaptic plasticity . Curr Opin Cell Biol . 1997;9:627–634
  14. Brummendorf T , Kenwrick S , Rathjen FG . Neural cell recognition molecule; L1: from cell biology to human hereditary brain malformations . Curr Opin Neurobiol . 1998;8:87–97
  15. Hortsch M , O'Shea KS , Zhao G , et al.  A conserved role for L1 as a transmembrane link between neuronal adhesion and membrane cytoskeleton assembly . Cell Adhes Commun . 1998;5:61–73
  16. Wachowiak R , Fiegel HC , Kaifi JT , Quaas A , Krickhahn A , Schurr PG , et al.  L1 is associated with favorable outcome in neuroblastomas in contrast to adult tumors . Ann Surg Oncol . 2007;14:3575–3580
  17. de Angelis E , MacFarlane J , Du JS , Yeo G , Hicks R , Rathjen FG , et al.  Pathological missense mutations of neural cell adhesion molecule L1 affect homophilic and heterophilic binding activities . EMBO J . 1999;18:4744–4753
  18. Oleszewski M, Beer S, Katich S, Geiger C, Zeller Y, Rauch U, et al. Integrin and neurocan binding to L1 involves distinct Ig domains . J Biol Chem . 1999;274:24602–24610
  19. Kaifi JT , Strelow A , Schurr PG , Reichelt U , Yekebas EF , Wachowiak R , et al.  L1 (CD171) is highly expressed in gastrointestinal stromal tumors . Mod Pathol . 2006;19:399–406
  20. Fogel M , Mechtersheimer S , Huszar M , Smirnov A , Abu-Dahi A , Tilgen W , et al.  L1 adhesion molecule (CD 171) in development and progression of human malignant melanoma . Cancer Lett . 2003;189:237–247
  21. Fogel M , Gutwein P , Mechtersheimer S , et al.  L1 expression as a predictor of progression and survival in patients with uterine and ovarian carcinomas . Lancet . 2003;362:869–875
  22. Gutwein P , Mechtersheimer S , Riedle S , Stoeck A , Gast D , Joumaa S , et al.  ADAM10-mediated cleavage of L1 adhesion molecule at the cell surface and in released membrane vesicles . FASEB J . 2003;17:292–294
  23. Kowitz A , Kadmon G , Verschueren H , Remels L , De Baetselier P , Hubbe M , et al.  Expression of L1 cell adhesion molecule is associated with lymphoma growth and metastasis . Clin Exp Metastasis . 1993;11:419–429
  24. Linnemann D , Raz A , Bock E . Differential expression of cell adhesion molecules in variants of K1735 melanoma cells differing in metastatic capacity . Int J Cancer . 1989;43:709–712
  25. Miyahara R , Tanaka F , Nakagawa T , Matsuoka K , Isii K , Wada H . Expression of neural cell adhesion molecules (polysialylated form of neural cell adhesion molecule and L1-cell adhesion molecule) on resected small cell lung cancer specimens: in relation to proliferation state . J Surg Oncol . 2001;77:49–54
  26. Thies A, Schachner M, Moll I, Berger J, Schulze HJ, Brunner G, et al. Overexpression of the cell adhesion molecule L1 is associated with metastasis in cutaneous malignant melanoma . Eur J Cancer . 2002;38:1708–1716
  27. Watson MA , Perry A , Tihan T , Prayson RA , Guha A , Bridge J , et al.  Gene expression profiling reveals unique molecular subtypes of neurofibromatosis type I–associated and sporadic malignant peripheral nerve sheath tumors . Brain Pathol . 2004;14:297–303
  28. Gutwein P , Oleszewski M , Mechtersheimer S , Agmon-Levin N , Krauss K , Altevogt P . Role of Src kinases in the ADAM-mediated release of L1 adhesion molecule from human tumor cells . J Biol Chem . 2000;275:15490–15497
  29. Kalus I , Schnegelsberg B , Seidah NG , Kleene R , Schachner M . The proprotein convertase PC5A and a metalloprotease are involved in the proteolytic processing of the neural adhesion molecule L1 . J Biol Chem . 2003;278:381–388
  30. Mechtersheimer S , Gutwein P , Agmon-Levin N , Stoeck A , Oleszewski M , Riedle S , et al.  Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins . J Cell Biol . 2001;155:661–673
  31. Montgomery AM , Becker JC , Siu CH , Lemmon VP , Cheresh DA , Pancook JD , et al.  Human neural cell adhesion molecule L1 and rat homologue Nile are ligands for integrin alpha ν beta 3 . J Cell Biol . 1996;132:475–485
  32. Allory Y , Matsuoka Y , Bazille C , Christensen EI , Ronco P , Debiec H . The L1 cell adhesion molecule is induced in renal cancer cells and correlates with metastasis in clear cell carcinomas . Clin Cancer Res . 2005;11:1190–1197
  33. Deichmann M , Kurzen H , Egner U , Altevogt P , Hartschuh W . Adhesion molecules CD171 (L1CAM) and CD24 are expressed by primary neuroendocrine carcinomas of the skin (Merkel cell carcinomas) . J Cutan Pathol . 2003;30:363–368
  34. Friedrich RE , Keiner D , Hagel C . Expression of insulin-like growth-factor-1 receptor (IGF-1R) in peripheral nerve sheath tumors in neurofibromatosis type 1 . Anticancer Res . 2007;27:2085–2090
  35. Takeuchi A , Ushigome S . Diverse differentiation in malignant peripheral nerve sheath tumours associated with neurofibromatosis-1: an immunohistochemical and ultrastructural study . Histopathology . 2001;39:298–309
  36. Khalifa MA , Montgomery EA , Ismiil N , Azumi N . What are the CD34+ cells in benign peripheral nerve sheath tumors? (Double immunostaining study of CD34 and S-100 protein) . Am J Clin Pathol . 2000;114:123–126
  37. Ariza A , Bilbao JM , Rosai J . Immunohistochemical detection of epithelial membrane antigen in normal perineurial cells and perineurioma . Am J Surg Pathol . 1988;12:678–683
  38. Hruban RH , Shiu MH , Senie RT , Woodruff JM . Malignant peripheral nerve sheath tumors of the buttock and lower extremity (A study of 43 cases) . Cancer . 1990;66:1253–1265
  39. Wong WW , Hirose T , Scheithauer BW , Schild SE , Gunderson LL . Malignant peripheral nerve sheath tumor: analysis of treatment outcome . Int J Radiat Oncol Biol Phys . 1998;42:351–360
  40. Huszar M , Moldenhauer G , Gschwend V , Ben-Arie A , Altevogt P , Fogel M . Expression profile analysis in multiple human tumors identifies L1 (CD171) as a molecular marker for differential diagnosis and targeted therapy . Hum Pathol . 2006;37:1000–1008
  41. Hoefnagel CA , Rutgers M , Buitenhuis CK , Smets LA , de Kraker J , Meli M , et al.  A comparison of targeting of neuroblastoma with mIBG and anti L1-CAM antibody mAb chCE7: therapeutic efficacy in a neuroblastoma xenograft model and imaging of neuroblastoma patients . Eur J Nucl Med . 2001;28:359–368
  42. Coindre JM , Trojani M , Contesso G , David M , Rouesse J , Bui NB , et al.  Reproducibility of a histopathologic grading system for adult soft tissue sarcoma . Cancer . 1986;58:306–309
  43. Costa J , Wesley RA , Glatstein E , Rosenberg SA . The grading of soft tissue sarcomas (Results of a clinicohistopathologic correlation in a series of 163 cases) . Cancer . 1984;53:530–541
  44. Maness PF , Schachner M . Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration . Nat Neurosci . 2007;10:19–26 Review. Erratum in: Nat Neurosci 2007;10(2):263.
  45. Guseva D , Angelov DN , Irintchev A , Schachner M . Ablation of adhesion molecule L1 in mice favours Schwann cell proliferation and functional recovery after peripheral nerve injury . Brain . 2009;132:2180–2195
  46. Maddaluno L , Verbrugge SE , Martinoli C , Matteoli G , Chiavelli A , Zeng Y , et al.  The adhesion molecule L1 regulates transendothelial migration and trafficking of dendritic cells . J Exp Med . 2009;206:623–635

 The first 2 authors contributed equally to this work.

 Supported by research grants from the “Deutsche Krebshilfe e.V.”/Dr. Mildred Scheel Stiftung” to J.T.K. and M.S.

PII: S1079-2104(11)00271-X

doi: 10.1016/j.tripleo.2011.04.019

Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology
Volume 113, Issue 2 , Pages 239-244 , February 2012