NK-1 receptor antagonists induce apoptosis and counteract substance P-related mitogenesis in human laryngeal cancer cell line HEp-2

Investigational New Drugs

Volumn 26, Issue 2, 2008, Pages 111-118

  Muñoz, Miguel ^a   Rosso, Marisa ^a   Aguilar, Francisco J ^a   González Moles, Miguel A ^b   Redondo, Maximino ^c   Esteban, Francisco ^a  

^a HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c HOSPITAL COSTA DEL SOL   (Spain)

Author keywords

Antineoplastic agents; Apoptosis; Human laryngeal carcinoma cell; L 732,138; L 733,060

Indexed keywords

3 [3,5 BIS(TRIFLUOROMETHYL)BENZYLOXY] 2 PHENYLPIPERIDINE; 4',6 DIAMIDINO 2 PHENYLINDOLE; N ACETYLTRYPTOPHAN 3,5 BIS(TRIFLUOROMETHYL)BENZYL ESTER; NEUROKININ 1 RECEPTOR; NEUROKININ 1 RECEPTOR ANTAGONIST; SUBSTANCE P; TETRAZOLIUM; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CELL COUNT; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LARYNX CANCER; MITOGENESIS; PRIORITY JOURNAL;

EID: 40549118238     PISSN: 01676997     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10637-007-9087-y     Document Type: Article

References (44)

1. 1. F Entschladen TL Drell 4th K Lang J Joseph KS Zaenker 2005 Neurotransmitters and chemokines regulate tumor cell migration: potential for a new pharmacological approach to inhibit invassion and metastasis development Curr Pharm Des 11 403 411 15723634 10.2174/1381612053382197 1:CAS:528:DC%2BD2MXhsVKnsrc%3D Entschladen F, Drell TL 4th, Lang K, Joseph J, Zaenker KS (2005) Neurotransmitters and chemokines regulate tumor cell migration: potential for a new pharmacological approach to inhibit invassion and metastasis development. Curr Pharm Des 11:403–411
2. 2. M Muñoz M Rosso JA Soult R Coveñas 2006 Antitumoural action of neurokinin-1 receptor antagonists on human brain cancer cell lines AV Yang Brain cancer: therapy and surgical intervention Nova Science New York 45 75 Muñoz M, Rosso M, Soult JA, Coveñas R (2006) Antitumoural action of neurokinin-1 receptor antagonists on human brain cancer cell lines. In: Yang AV (ed) Brain cancer: therapy and surgical intervention. New York: Nova Science, pp 45–75
3. 3. US Euler von JH Gaddum 1931 An unidentified depressor substance in certain tissue extracts J Physiol 72 74 87 von Euler US, Gaddum JH (1931) An unidentified depressor substance in certain tissue extracts. J Physiol 72:74–87
4. 4. B Pernow 1983 Substance P Pharmacol Rev 35 85 141 6196797 1:CAS:528:DyaL2cXnsVE%3D Pernow B (1983) Substance P. Pharmacol Rev 35:85–141
5. 5. T Hökfelt B Pernow J Wahren 2001 Substance P: a pioneer amongst neuropeptides J Intern Med 249 27 40 11168782 10.1046/j.0954-6820.2000.00773.x Hökfelt T, Pernow B, Wahren J (2001) Substance P: a pioneer amongst neuropeptides. J Intern Med 249:27–40
6. 6. W Luo TR Sharif M Sharif 1996 Substance P-induced mitogenesis in human astrocytoma cells correlates with activation of the mitogen-activated protein kinase signaling pathway Cancer Res 56 4983 4991 8895754 1:CAS:528:DyaK28XmsFygt7w%3D Luo W, Sharif TR, Sharif M (1996) Substance P-induced mitogenesis in human astrocytoma cells correlates with activation of the mitogen-activated protein kinase signaling pathway. Cancer Res 56:4983–4991
7. 7. TR Sharif W Luo PJ Houghron M Sharif 1996 Substance K peptide induces mitogenesis by activating the mitogen-activated protein kinase signalling pathway through the substance P receptor (NK-1 subtype) in human astrocytoma Cell Pharmacol 3 441 449 1:CAS:528:DyaK2sXktlejt74%3D Sharif TR, Luo W, Houghron PJ, Sharif M (1996) Substance K peptide induces mitogenesis by activating the mitogen-activated protein kinase signalling pathway through the substance P receptor (NK-1 subtype) in human astrocytoma. Cell Pharmacol 3:441–449
8. 8. C Palma F Nardelli S Manzini CA Maggi 1999 Substance P activates responses correlated with tumour growth in human glioma cell lines bearing tachykinin NK1 receptors Br J Cancer 79 236 243 9888463 1:CAS:528:DyaK1MXmvFehtQ%3D%3D Palma C, Nardelli F, Manzini S, Maggi CA (1999) Substance P activates responses correlated with tumour growth in human glioma cell lines bearing tachykinin NK1 receptors. Br J Cancer 79:236–243
9. 9. M Muñoz A Pérez M Rosso C Zamarriego R Rosso 2004 Antitumoural action of NK1 receptor antagonist L-733,060 on human melanoma cell lines Melanoma Res 14 183 188 15179186 10.1097/01.cmr.0000129376.22141.a3 1:CAS:528:DC%2BD2cXksF2ls7o%3D Muñoz M, Pérez A, Rosso M, Zamarriego C, Rosso R (2004) Antitumoural action of NK1 receptor antagonist L-733,060 on human melanoma cell lines. Melanoma Res 14:183–188
10. 10. M Muñoz M Rosso A Pérez R Coveñas R Rosso C Zamarriego JI Piruat 2005 The NK1 receptor is involved in the antitumoural action of L-733,060 and in the mitogenic action of substance P on neuroblastoma and glioma cell lines Neuropeptides 39 427 432 15939468 10.1016/j.npep.2005.03.004 1:CAS:528:DC%2BD2MXmvVGisbc%3D Muñoz M, Rosso M, Pérez A, Coveñas R, Rosso R, Zamarriego C, Piruat JI (2005) The NK1 receptor is involved in the antitumoural action of L-733,060 and in the mitogenic action of substance P on neuroblastoma and glioma cell lines. Neuropeptides 39:427–432
11. 11. M Muñoz M Rosso R Coveñas 2006 The NK-1 receptor is involved in the antitumoural action of L-733,060 and in the mitogenic action of substance P on human pancreatic cancer cell lines Lett Drug Des Discov 3 323 329 10.2174/157018006777574168 Muñoz M, Rosso M, Coveñas R (2006) The NK-1 receptor is involved in the antitumoural action of L-733,060 and in the mitogenic action of substance P on human pancreatic cancer cell lines. Lett Drug Des Discov 3:323–329
12. 12. M Ziche L Morbidelli M Pacini P Gepetti G Alessandri CA Maggi 1990 Substance P stimulates neovascularization in vivo and proliferation of cultured endothelial cells Microvasc Res 40 264 278 1701206 10.1016/0026-2862(90)90024-L 1:CAS:528:DyaK3MXhslyksbY%3D Ziche M, Morbidelli L, Pacini M, Gepetti P, Alessandri G, Maggi CA (1990) Substance P stimulates neovascularization in vivo and proliferation of cultured endothelial cells. Microvasc Res 40:264–278
13. 13. K Lang TL Drell A Lindecke B Niggemann C Kaltschmidt KS Zaenker F Entschladen 2004 Induction of a metastatogenic tumor cell type by neurotransmitters and its pharmacological inhibition by established drugs Int J Cancer 112 231 238 15352035 10.1002/ijc.20410 1:CAS:528:DC%2BD2cXnvVejsL8%3D Lang K, Drell TL, Lindecke A, Niggemann B, Kaltschmidt C, Zaenker KS, Entschladen F (2004) Induction of a metastatogenic tumor cell type by neurotransmitters and its pharmacological inhibition by established drugs. Int J Cancer 112:231–238
14. 14. T Harrison BJ Willians CJ Swain RG Ball 1994 Piperidine-ether based hNK1 antagonists 1: determination of the relative and absolute stereochemical requirements Bioorg Med Chem Lett 4 2545 2550 10.1016/S0960-894X(01)80280-8 1:CAS:528:DyaK2MXit1Orsr8%3D Harrison T, Willians BJ, Swain CJ, Ball RG (1994) Piperidine-ether based hNK1 antagonists 1: determination of the relative and absolute stereochemical requirements. Bioorg Med Chem Lett 4:2545–2550
15. 15. NM Rupniak E Carlson S Boyce JK Webb RG Hill 1996 Enantioselective inhibition of the formalin paw late phase by the NK1 receptor antagonist L-733,060 in gerbils Pain 67 189 195 8895247 10.1016/0304-3959(96)03109-0 1:CAS:528:DyaK28XmsFCgurg%3D Rupniak NM, Carlson E, Boyce S, Webb JK, Hill RG (1996) Enantioselective inhibition of the formalin paw late phase by the NK1 receptor antagonist L-733,060 in gerbils. Pain 67:189–195
16. 16. MS Kramer N Cutler J Feighner R Shrivastava J Carman JJ Sramek SA Reines G Liu D Snavely E Wyatt-Knowles JJ Halle 1998 Distinct mechanism for antidepressant activity by blockade of central substance P receptors Science 281 1640 1645 9733503 10.1126/science.281.5383.1640 1:CAS:528:DyaK1cXmtVSqtb0%3D Kramer MS, Cutler N, Feighner J, Shrivastava R, Carman J, Sramek JJ, Reines SA, Liu G, Snavely D, Wyatt-Knowles E, Halle JJ (1998) Distinct mechanism for antidepressant activity by blockade of central substance P receptors. Science 281:1640–1645
17. 17. GB Varty ME Cohen-Williams JC Hunter 2003 The antidepressant-like effects of neurokinin NK1 receptor antagonists in a gerbil tail suspension test Behav Pharmacol 14 87 95 12576885 1:CAS:528:DC%2BD3sXht1Cmsb8%3D Varty GB, Cohen-Williams ME, Hunter JC (2003) The antidepressant-like effects of neurokinin NK1 receptor antagonists in a gerbil tail suspension test. Behav Pharmacol 14:87–95
18. 18. NM Rupniak EC Carlson T Harrison B Oates E Seward S Owen C Felipe de S Hunt A Wheeldon 2000 Pharmacological blockade or genetic deletion of substance P (NK(1)) receptors attenuates neonatal vocalisation in guinea-pigs and mice Neuropharmacology 39 1413 1421 10818257 10.1016/S0028-3908(00)00052-6 1:CAS:528:DC%2BD3cXjt1alsbk%3D Rupniak NM, Carlson EC, Harrison T, Oates B, Seward E, Owen S, de Felipe C, Hunt S, Wheeldon A (2000) Pharmacological blockade or genetic deletion of substance P (NK(1)) receptors attenuates neonatal vocalisation in guinea-pigs and mice. Neuropharmacology 39:1413–1421
19. 19. R Bang G Sass AK Kiemer AM Vollmar WL Neuhuber G Tiegs 2003 Neurokinin-1 receptor antagonists CP-96,345 and L-733,060 protect mice from cytokine-mediated liver injury J Pharmacol Exp Ther 305 31 39 12649350 10.1124/jpet.102.043539 1:CAS:528:DC%2BD3sXis1antLg%3D Bang R, Sass G, Kiemer AK, Vollmar AM, Neuhuber WL, Tiegs G (2003) Neurokinin-1 receptor antagonists CP-96,345 and L-733,060 protect mice from cytokine-mediated liver injury. J Pharmacol Exp Ther 305:31–39
20. 20. PJ Woll E Rozengurt 1988 [D-Arg 1–D-Phe 5, D-Trp 7, 9, Leu 11 ] Substance P, a potent bombesin antagonist in murine Swiss 3T3 cells, inhibits the growth of human small cell lung cancer cells in vitro Proc Natl Acad Sci U S A 35 1859 1863 10.1073/pnas.85.6.1859 Woll PJ, Rozengurt E (1988) [D-Arg 1–D-Phe 5, D-Trp 7, 9, Leu 11 ] Substance P, a potent bombesin antagonist in murine Swiss 3T3 cells, inhibits the growth of human small cell lung cancer cells in vitro. Proc Natl Acad Sci U S A 35:1859–1863
21. 21. S Langdon T Sethi A Richie M Muir J Smyth E Rozengurt 1992 Broad spectrum neuropeptide antagonists inhibit the growth of small cell lung cancer in vivo Cancer Res 52 4554 4557 1379515 1:CAS:528:DyaK38Xmt1Grsbw%3D Langdon S, Sethi T, Richie A, Muir M, Smyth J, Rozengurt E (1992) Broad spectrum neuropeptide antagonists inhibit the growth of small cell lung cancer in vivo. Cancer Res 52:4554–4557
22. 22. JG Reeve NM Bleehen 1994 [D-Arg 1–D-Phe 5, D-Trp 7, 9, Leu 11 ] Substance P induces apoptosis in lung cancer cell lines in vitro Biochem Biophys Res Com 199 1313 1319 7511895 10.1006/bbrc.1994.1374 1:CAS:528:DyaK2cXitlKrtrw%3D Reeve JG, Bleehen NM (1994) [D-Arg 1–D-Phe 5, D-Trp 7, 9, Leu 11 ] Substance P induces apoptosis in lung cancer cell lines in vitro. Biochem Biophys Res Com 199:1313–1319
23. 23. MJ Seckl T Higgins F Wildmer E Rozengurt 1997 [D-Arg 1, D-Trp 5,7, 9, Leu 11 ] Substance P: a novel potent inhibitor of signal transduction and growth in vitro and in vivo in small cell lung cancer cells Cancer Res 57 51 54 8988040 1:CAS:528:DyaK2sXjvFGiug%3D%3D Seckl MJ, Higgins T, Wildmer F, Rozengurt E (1997) [D-Arg 1, D-Trp 5,7, 9, Leu 11 ] Substance P: a novel potent inhibitor of signal transduction and growth in vitro and in vivo in small cell lung cancer cells. Cancer Res 57:51–54
24. 24. C Palma M Bigioni C Irrissuto F Nardelli CA Maggi S Manzini 2000 Anti-tumour activity of tachykinin NK1 receptor antagonists on human glioma U373 MG xenograft Br J Cancer 82 480 487 10646908 10.1054/bjoc.1999.0946 1:CAS:528:DC%2BD3cXpt12htQ%3D%3D Palma C, Bigioni M, Irrissuto C, Nardelli F, Maggi CA, Manzini S (2000) Anti-tumour activity of tachykinin NK1 receptor antagonists on human glioma U373 MG xenograft. Br J Cancer 82:480–487
25. 25. M Muñoz M Rosso A Pérez R Coveñas R Rosso C Zamarriego JA Soult I Montero 2005 Antitumoural action of the neurokinin-1-receptor antagonist L-733,060 and mitogenic action of substance P on human retinoblastoma cell lines Invest Ophthalmol Vis Sci 46 2567 2570 15980249 10.1167/iovs.04-1530 Muñoz M, Rosso M, Pérez A, Coveñas R, Rosso R, Zamarriego C, Soult JA, Montero I (2005) Antitumoural action of the neurokinin-1-receptor antagonist L-733,060 and mitogenic action of substance P on human retinoblastoma cell lines. Invest Ophthalmol Vis Sci 46:2567–2570
26. 26. M Muñoz A Pérez R Coveñas M Rosso E Castro 2004 Antitumoural action of L-733,060 on neuroblastoma and glioma cell lines Arch Ital Biol 142 105 112 15248566 Muñoz M, Pérez A, Coveñas R, Rosso M, Castro E (2004) Antitumoural action of L-733,060 on neuroblastoma and glioma cell lines. Arch Ital Biol 142:105–112
27. 27. AM MacLeod KJ Merchant F Brookfield F Kelleher G Stevenson AP Owens CJ Swain MA Cascieri S Sadowski E Ber CD Strader TM Fong 1994 Identification of L-tryptophan derivatives with potent and selective antagonist activity at the NK1 receptor J Med Chem 37 1269 1274 7513763 10.1021/jm00035a006 1:CAS:528:DyaK2cXksFOqsrg%3D MacLeod AM, Merchant KJ, Brookfield F, Kelleher F, Stevenson G, Owens AP, Swain CJ, Cascieri MA, Sadowski S, Ber E, Strader CD, Fong TM (1994) Identification of L-tryptophan derivatives with potent and selective antagonist activity at the NK1 receptor. J Med Chem 37:1269–1274
28. 28. CM Cahill TJ Coderre 2002 Attenuation of hyperalgesia in a rat model of neuropathic pain after intrathecal pre-or post-treatment with a neurokinin-1 antagonist Pain 95 277 285 11839427 10.1016/S0304-3959(01)00410-9 1:CAS:528:DC%2BD38Xht1agsb4%3D Cahill CM, Coderre TJ (2002) Attenuation of hyperalgesia in a rat model of neuropathic pain after intrathecal pre-or post-treatment with a neurokinin-1 antagonist. Pain 95:277–285
29. 29. MA Hossen Y Fujii Y Sugimoto R Kayasuga C Kamei 2003 Histamine H3 receptors regulate vascular permeability changes in the skin of mast cell-deficient mice Int Immunopharmacol 3 1563 1568 14555281 10.1016/S1567-5769(03)00009-2 1:CAS:528:DC%2BD3sXnvVKksr0%3D Hossen MA, Fujii Y, Sugimoto Y, Kayasuga R, Kamei C (2003) Histamine H3 receptors regulate vascular permeability changes in the skin of mast cell-deficient mice. Int Immunopharmacol 3:1563–1568
30. 30. M Muñoz M Rosso R Coveñas I Montero MA González-Moles MJ Robles 2007 Neurokinin-1 receptors located in human retinoblastoma cell lines: antitumor action of its antagonists, L-732,138 Invest Ophthalmol Vis Sci 48 2775 2781 17525212 10.1167/iovs.05-1591 Muñoz M, Rosso M, Coveñas R, Montero I, González-Moles MA, Robles MJ (2007) Neurokinin-1 receptors located in human retinoblastoma cell lines: antitumor action of its antagonists, L-732,138. Invest Ophthalmol Vis Sci 48:2775–2781
31. 31. M Muñoz M Rosso R Coveñas 2007 NK-1 receptor antagonists as new anti-tumoural agents: action on human neuroblastoma cell lines JA Fernandes Focus on neuroblastoma research Nova Science New York 31 56 Muñoz M, Rosso M, Coveñas R (2007) NK-1 receptor antagonists as new anti-tumoural agents: action on human neuroblastoma cell lines. In: Fernandes JA (ed) Focus on neuroblastoma research. Nova Science, New York, pp. 31–56
32. 32. L Caberlotto YL Hurd P Murdock JP Wahlin S Melotto M Corsi R Carletti 2003 Neurokinin 1 receptor and relative abundance of the short and long isoforms in the human brain Eur J Neurosci 17 1736 1746 12752772 10.1046/j.1460-9568.2003.02600.x Caberlotto L, Hurd YL, Murdock P, Wahlin JP, Melotto S, Corsi M, Carletti R (2003) Neurokinin 1 receptor and relative abundance of the short and long isoforms in the human brain. Eur J Neurosci 17:1736–1746
33. 33. JP McGillis ML Organist KH Scriven DG Payan 1987 Purification of the 33,000-dalton ligand binding-protein constituent of the lymphoblast substance P receptor J Neurosci Res 18 1 190 194 2824800 10.1002/jnr.490180127 1:CAS:528:DyaL1cXntVyrtQ%3D%3D McGillis JP, Organist ML, Scriven KH, Payan DG (1987) Purification of the 33,000-dalton ligand binding-protein constituent of the lymphoblast substance P receptor. J Neurosci Res 18(1):190–194
34. 34. JP McGillis M Mitsuhashi DG Payan 1990 Immunomodulation by tachykinin neuropeptides Ann N Y Acad Sci 594 85 94 1696081 10.1111/j.1749-6632.1990.tb40470.x 1:CAS:528:DyaK3MXktVSrtbo%3D McGillis JP, Mitsuhashi M, Payan DG (1990) Immunomodulation by tachykinin neuropeptides. Ann N Y Acad Sci 594:85–94
35. 35. H Friess Z Zhu V Liard X Shi SV Shrikhande L Wang K Lieb M Korc C Palma A Zimmermann JC Reubi MW Buchler 2003 Neurokinin-1 receptor expression and its potential effects on tumor growth in human pancreatic cancer Lab Invest 83 731 742 12746482 1:CAS:528:DC%2BD3sXjtlKjs7o%3D Friess H, Zhu Z, Liard V, Shi X, Shrikhande SV, Wang L, Lieb K, Korc M, Palma C, Zimmermann A, Reubi JC, Buchler MW (2003) Neurokinin-1 receptor expression and its potential effects on tumor growth in human pancreatic cancer. Lab Invest 83:731–742
36. 36. A Tarkkanen T Tervo K Tervo L Eränkö O Eränkö AC Cuello 1983 Substance P immunoreactivity in normal human retina and in retinoblastoma Ophthalmic Res 15 300 306 6199710 1:CAS:528:DyaL2cXhtFyksbY%3D 10.1159/000265276 Tarkkanen A, Tervo T, Tervo K, Eränkö L, Eränkö O, Cuello AC (1983) Substance P immunoreactivity in normal human retina and in retinoblastoma. Ophthalmic Res 15:300–306
37. 37. CM Lee W Kum CS Cockram R Teoh JD Young 1989 Functional substance P receptors on a human astrocytoma cell line (U-373 MG) Brain Res 488 328 331 2545304 10.1016/0006-8993(89)90724-5 1:CAS:528:DyaL1MXksFSqtb0%3D Lee CM, Kum W, Cockram CS, Teoh R, Young JD (1989) Functional substance P receptors on a human astrocytoma cell line (U-373 MG). Brain Res 488:328–331
38. 38. VK Khare AP Albino JA Reed 1998 The neuropeptide/mast cell secretagogue substance P is expressed in cutaneus melanocytic lesions J Cutan Pathol 25 2 10 9508337 10.1111/j.1600-0560.1998.tb01682.x 1:STN:280:DyaK1c7mslOlsA%3D%3D Khare VK, Albino AP, Reed JA (1998) The neuropeptide/mast cell secretagogue substance P is expressed in cutaneus melanocytic lesions. J Cutan Pathol 25:2–10
39. 39. D Singh DD Joshi M Hameed J Qian P Gascón PB Maloof A Mosenthal P Rameshwar 2000 Increased expression of preprotachykinin-I and neurokinin receptors in human breast cancer cells: implications for bone marrow metastasis Proc Natl Acad Sci U S A 97 388 393 10618428 10.1073/pnas.97.1.388 1:CAS:528:DC%2BD3cXjvVGhtQ%3D%3D Singh D, Joshi DD, Hameed M, Qian J, Gascón P, Maloof PB, Mosenthal A, Rameshwar P (2000) Increased expression of preprotachykinin-I and neurokinin receptors in human breast cancer cells: implications for bone marrow metastasis. Proc Natl Acad Sci U S A 97:388–393
40. 40. F Esteban M Munoz MA González-Moles M Rosso 2006 A role for substance P in carcinogenesis; a mechanism to counteract intracellular death signals following oncogene activation or DNA damage Cancer Metastasis Rev 25 137 145 16680578 10.1007/s10555-006-8161-9 1:CAS:528:DC%2BD28Xktlaksrg%3D Esteban F, Munoz M, González-Moles MA, Rosso M (2006) A role for substance P in carcinogenesis; a mechanism to counteract intracellular death signals following oncogene activation or DNA damage. Cancer Metastasis Rev 25:137–145
41. 41. P Diemunsch L Grelot 2000 Potential of substance P antagonists as antiemetics Drugs 60 533 546 11030465 10.2165/00003495-200060030-00002 1:CAS:528:DC%2BD3cXntlymu7c%3D Diemunsch P, Grelot L (2000) Potential of substance P antagonists as antiemetics. Drugs 60:533–546
42. 42. GAM Giardina S Gagliardi M Martinelli 2003 Antagonists at the neurokinin receptors—recent patent literature Drugs 6 758 772 1:CAS:528:DC%2BD3sXnvVGkurc%3D Giardina GAM, Gagliardi S, Martinelli M (2003) Antagonists at the neurokinin receptors—recent patent literature. Drugs 6:758–772
43. 43. M Nowicki B Miskowiak 2002 Comparison of the cell immunophenotype of metastatic and primary foci in stage IV-S neuroblastoma Folia Histochem Cytobiol 40 297 303 12219840 Nowicki M, Miskowiak B (2002) Comparison of the cell immunophenotype of metastatic and primary foci in stage IV-S neuroblastoma. Folia Histochem Cytobiol 40:297–303
44. 44. IM Hennig JA Laissue U Horisberger JC Reubi 1995 Substance-P receptors in human primary neoplasms: tumoral and vascular localization Int J Cancer 61 786 792 7790112 10.1002/ijc.2910610608 1:STN:280:DyaK2MzhtVSmtw%3D%3D Hennig IM, Laissue JA, Horisberger U, Reubi JC (1995) Substance-P receptors in human primary neoplasms: tumoral and vascular localization. Int J Cancer 61:786–792