A role for substance P in cancer promotion and progression: A mechanism to counteract intracellular death signals following oncogene activation or DNA damage

Cancer and Metastasis Reviews

Volumn 25, Issue 1, 2006, Pages 137-145

  Esteban, F ^a   Munoz M ^a   Gonzalez Moles M A ^b   Rosso, M ^a  

^a HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

Antitumor; Carcinogenesis; G protein coupled receptor; Neurokinin 1 receptor; Neurokinin 1 receptor antagonists; Oncogenesis; Substance P

Indexed keywords

3 [3,5 BIS(TRIFLUOROMETHYL)BENZYLOXY] 2 PHENYLPIPERIDINE; G PROTEIN COUPLED RECEPTOR; N ACETYLTRYPTOPHAN 3,5 BIS(TRIFLUOROMETHYL)BENZYL ESTER; NEUROKININ 1 RECEPTOR; NEUROKININ 1 RECEPTOR ANTAGONIST; SUBSTANCE P; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER; CANCER GROWTH; CANCER THERAPY; CARCINOGENESIS; DNA DAMAGE; DOSE RESPONSE; GENE ACTIVATION; HUMAN; MITOGENESIS; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR PROMOTION;

ANTINEOPLASTIC AGENTS; APOPTOSIS REGULATORY PROTEINS; DISEASE PROGRESSION; DNA DAMAGE; GROWTH SUBSTANCES; HUMANS; NEOPLASMS; ONCOGENES; RECEPTORS, NEUROKININ-1; SIGNAL TRANSDUCTION; SUBSTANCE P; TACHYKININS;

EID: 33646558897     PISSN: 01677659     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10555-006-8161-9     Document Type: Review

References (93)

1. Hahn WC, Weinberg RA: Mechanisms of disease: rules for making human tumor cells. N Engl J Med 347: 1593-1603, 2002
2. Rollandy I, Dreux C, Imhoff V, Rossignol B: Importance of the presence of the N-terminal tripeptide of substance P for the stimulation of phosphatidylinositol metabolism in rat parotid gland: a possible activation of phospholipases C and D. Neuropeptides 13: 175-185, 1989
3. Pradier L, Heuillet E, Hubert JP, Laville M, Le Guern S, Doble A: J Neurochem 61: 1850-1858, 1993
4. Luo W, Sharif TR, Sharif M: Substance P-induced mitogenesis in human astrocytoma cells correlates with activation of the mitogen-activated protein kinase signaling pathway. Cancer Res 56:4983-4991, 1996
5. DeFea KA, Zalevsky J, Thoma MS, De'ry O, Mullins RD, Bunnett NW: Beta-arrestin-dependent endocytosis of proteinase-activated receptor 2 is required for intracellular targeting of activated ERK1/2. J Cell Biol 148: 1267-1282, 2000
6. Van den Broeck J, Torfs H, Poels J, Van Poyer W, Swinnen E, Ferket K, De Loof A: Tachykinin-like peptides and their receptors. A review. Ann NY Acad Sci 897:374-387, 1999
7. Patacchini R, Maggi CA: Peripheral tachykinin receptors as targets for new drugs. Eur J Pharmacol 429(1-3): 13-21, 2001
8. Khawaja AM, Rogers DF: Tachykinins: receptor to effector. Int J Biochem Cell Biol 28: 721-738, 1996
9. Quartara L, Maggi CA: The tachykinin NK1 receptor. Part II: distribution and pathophysiological roles. Neuropeptides 32:1-49, 1998
10. Guo CJ, Lai JP, Luo HM, Douglas SD, Ho WZ: Substance P upregulates macrophage inflammatory protein-1 beta expression in human T lymphocytes. J Neuroimmunol 131(1-2): 160-167, 2002
11. Fiebich BL, Schleicher S, Butcher RD, Craig A, Lieb K: The neuropeptide substance P activates p38 mitogen-activated protein kinase resulting in IL-6 expression independently from NF-kappa B. J Immunol 165(10): 5606-5611, 2000
12. Castagliuolo I, Valenick L, Liu J, Pothoulakis C: Epidermal growth factor receptor transactivation mediates substance P-induced mitogenic responses in U-373 MG cells. J Biol Chem 275: 26545-26550, 2000
13. McGillis JP, Mitsuhashi M, Payan DG: Immunomodulation by tachykinin neuropeptides. Ann NY Acad Sci 594:85-94, 1990
14. Goetzl EJ, Sreedharan SP: Mediators of communication and adaptation in the neuroendocrine and immune systems. FASEB J 6(9):2646-2652, 1992
15. Lambrecht BN: Immunologists getting nervous: neuropeptides, dendritic cells and T cell activation. Respir Res 2(3): 133-138, 2001
16. Rozengurt E: Neuropeptides as growth factors for normal and cancerous cells. Trends Endocrinol Metab 13(3): 128-134, 2002
17. von Euler US, Gaddum JH: An unidentified depressor substance in certain tissue extracts. J Physiol 72:74-87, 1931
18. DeVane CL: Substance P: a new era, a new role. Pharmacotherapy 21(9): 1061-1069, 2001
19. Culman J, Unger T: Central tachykinins: mediators of defence reaction and stress reactions. Can J Physiol Pharmacol 73(7):885-891, 1995
20. De Felipe C, Herrero JF, O'Brien JA, Palmer JA, Doyle CA, Smith AJ, Laird JM, Belmonte C, Cervero F, Hunt SP: Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature 392(6674):394-397, 1998
21. Mantyh PW: Substance P and the inflammatory and immune response. Ann NY Acad Sci 632:263-271, 1991
22. Harrison S, Geppetti P: Substance P. Int J Biochem Cell Biol 33:555-576, 2001
23. Chahl LA, Ladd RJ: Local oedema and general excitation of cutaneous sensory receptors produced by electrical stimulation of the saphenous nerve in the rat. Pain 2:25-34, 1976
24. Lembeck F, Holzer P: Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn-Schmiedeberg's Arch Pharmacol 310:175-183, 1979
25. Furness J, Papka RE, Della NG, Costa M, Eskay RL: Substance P-like immunoreactivity in nerves associated with the vascular system of guinea-pigs Neuroscience 7:447-459, 1982
26. Lundberg JM, Brodin E, Hua X, Saria A. Vascular permeability changes and smooth muscle contraction in relation to capsaicinsensitive substance P afferents in the guinea-pig. Acta Physiol Scand 120:217-227, 1984
27. Pascual DW, Xu-Amano J, Kiyono H, McGhee JR, Bost KL: Substance P acts directly upon cloned B Lymphoma cells to enhace IgA and IgM production. J Immunol 146:2130-2136, 1991
28. Feistritzer C, Clausen J, Sturn DH, Djanani A, Gunsilius E, Wiedermann CJ, Kahler CM: Natural killer cell functions mediated by the neuropeptide substance P. Regul Pep 116:119-126, 2003
29. Lieb K, Fiebich BL, Berger M, Bauer J, Schulze-Osthoff K: The neuropeptide substance P activates transcription factors NF.kB and kB-dependent gene expression in human astrocytoma cells. J Immunol 159:4952-4958, 1997
30. Muñoz M, Pérez A, Rosso M, Zamarriego C, Rosso R: Antitumoural action of NK1 receptor antagonist L-733,060 on human melanoma cell lines. Melanoma Res 14:183-188, 2004b
31. Walsh DT, Weg VB, Williams TJ, Nourshargh S: Substance P induced inflammatory responses in guinea-pig skin: the effect of specific NK1 receptor antagonists and the role of endogenous mediators. Br J Pharmacol 114:1343-1350, 1995
32. Weinstock JV, Blum A, Walden J, Walden T: Eosinophils from granulomas in murine Schistosomiasis mansoni produce SP. J Immunology 141:961-966, 1998
33. Cook GA, Elliott D, Metwali A, Blu AM, Sandor M, Lynch R, Weinstock JV: Molecular evidence that granuloma T lymphocytes in murine Schistosomiasis mansoni express an authentic SP (NK1) receptor. J Immunology 152:1830-1835, 1994
34. Keranen U, Jarvinen H, Kiviluoto T, Kivilaakso E, Soinila S: Substance P and VIP-immunoreactive innervation in normal and inflamed pouches after restorative proctocolectomy for ulcerative colitis. Dig Dis Sci 41:1658-1664, 1996
35. Keranen U, Jarvinen H, Karkkaine P, Kiviluoto T, Kivilaakso E, Soinila S: Substance P - an underlying factor for pouchitis?. Prospective study of substance P and VIP-immunoreactive innervation and mast cells. Dig Dis Sci 41:1665-1671, 1996
36. Payan DG, Brewster DR, Missirian-Bastian A, Goetzl EJ: Substance P recognition of a subset of human T lymphocytes. J Clin Invest 74:1532-1539, 1984
37. Hepler JR, Gilman AC: G proteins. Trends Biochem Sci 17: 383-387, 1992
38. Clapham D, Neer EJ: New roles: G protein βγ-dimers in transmembrane signalling. Nature 365: 406, 1993
39. Horstmann S, Kahle PJ, Borasio GD: Inhibitors of p38 mitogen-activated protein kinase promote neuronal survival in vitro J. Neurosci Res 52: 483-490, 1998
40. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME: Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270: 1326-1331, 1995
41. Daaka Y, Luttrell LM, Lefkowitz RJ: Switching of the coupling of the beta2-adrenergic receptor to different G proteins by protein kinase A. Nature 390: 88-91, 1997
42. DeFea KA, Vaughn ZD, O'Bryan EM, Nishijima D, Dery O, Bunnett NW: The proliferative and antiapoptotic effects of substance P are facilitated by formation of a beta-arrestin-dependent scaffolding complex. Proc Natl Acad Sci USA 97(20): 11086-11091, 2000
43. Luttrell LM, Ferguson SS, Daaka Y, Miller WE, Maudsley S, Della Rocca GJ, Lin F, Kawakatsu H, Owada K, Luttrell DK, Caron MG, Lefkowitz RJ: Beta-arrestin-dependent formation of beta2 adrenergic receptor-Src protein kinase complexes. Science 283: 655-661, 1999
44. van Biesen T, Hawes BE, Raymond JR, Luttrell LM, Koch WJ, Lefkowitz RJ: G(o)-protein alpha-subunits activate mitogen-activated protein kinase via a novel protein kinase C-dependent mechanism. J Biol Chem 271(3): 1266-1269, 1996
45. Ignatova EG, Belcheva MM, Bohn LM, Neuman MC, Coscia CJ: Requirement of receptor internalization for opioid stimulation of mitogen-activated protein kinase: biochemical and immunofluorescence confocal microscopic evidence. J Neurosci 19: 56-63, 1999
46. Vögler O, Nolte B, Voss M, Schmidt M, Jakobs KH, van Koppen CJ: Regulation of muscarinic acetylcholine receptor sequestration and function by beta-arrestin. J Biol Chem 274: 12333-12338, 1999
47. Koon HW, Zhao D, Na X, Moyer MP, Pothoulakis C: Metallo-proteinases and transforming growth factor-β mediate substance p-induced mitogen-activated protein kinase activation and proliferation in human Colonocytes. J Biol Chem 279: 45519-45527, 2004
48. Parma J, Duprey L, Van Sande J, Cochaux P, Gervy C, Mochel J, Dumont J, Vassart G: Somatic mutations in the thyrotropin receptor gene cause hyperfunctioning thyroid adenomas. Nature 365: 649-651, 1993
49. Daub H, Wallasch C, Lankenau A, Herrlich A, Ullrich A: Signal characteristics of G protein-transactivated EGF receptor. EMBO J 16: 7032-7044, 1997
50. Friess H, Zhu Z, Liard V, Shi X, Shrikhande SV, Wang L, Lieb K, Korc M, Palma C, Zimmermann A, Reubi JC, Buchler MW: Neurokinin-1 receptor expression and its potential effects on tumor growth in human pancreatic cancer. Lab Invest 83:731-742, 2003
51. Palma C, Nardelli F, Manzini S, Maggi CA: Substance P activates responses correlated with tumour growth in human glioma cells line bearing tachykinin NK1 receptors. Br J Cancer 79:236-243, 1999
52. Muñoz M, Pérez A, Coveñas R, Rosso M, Castro E: Antitumoural action of L-733,060 on neuroblastoma and glioma cell lines. Arch Ital Biol 142:105-112, 2004a
53. Singh D, Joshi DD, Hameed M, Qian J, Gascon P, Maloof PB, Mosenthal A, Rameshwar P: Increased expression of preprotachykinin-I and neurokinin receptors in human breast cancer cells: implications for bone marrow metastasis. Proc Natl Acad Sci USA 97: 388-393, 2000
54. Sitohy B, El Salhy M: Changes in the colonic enteric nervous system in rats with chemically induced colon dysplasia and carcinoma. Acta Oncol 41:543-549, 2002
55. Payan DG, Brewster DR, Goetzl EJ: Specific stimulation of human T lymphocytes by substance P. J Immunol 131:1613-1615, 1983
56. Nilsson J, von Euler AM, Dalsgaard CJ: Stimulation of connective tissue cell growth by substance P and substance K. Nature 315:61-63, 1985
57. Lotz M, Carson DA, Vaughan JH: Substance P activation of rheumatoid synoviocytes: neural pathway in pathogenesis of arthritis. Science 235:893-895, 1987
58. Ziehe M, Morbidelli L, Pacini M, Dolara P, Maggi CA: NK1-receptors mediate the proliferative response of human fibroblasts to tachykinins. Br J Pharmacol 100:11-14, 1990
59. Sharif TR, Luo W, Houghron PJ, Sharif M. 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, 1996
60. Muñoz M, Rosso M, Pérez A, Coveñas R, Rosso R, Zamarriego C, Piruat JI: 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(4): 427-32, 2005a
61. Muñoz M, Rosso M, Pérez A, Coveñas R, Rosso R, Zamarriego C, Soult JA, Montera I. 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, 2005b
62. Fowler CJ, Brannstrom G: Substance P enhances forskolin-stimulated cyclic AMP production in human UC11MG astrocytoma cells. Methods Find Exp Clin Pharmacol 16:21-28, 1994
63. Globus M, Smith MJ, Vethamany-Globus S: Evidence supporting a mitogenic role for substance P in amphibian limb regeneration. Ann NY Acad Sci 632:396-399, 1991
64. Salo E, Baguna T: Stimulation of cellular proliferation and differentiation in the intact and regenerating planarian Dugesia(G) tigrina by the neuropeptide substance P. J Exp Zool 237:129-135, 1986
65. Lee CM, Kum W, Cockram CS, Teoh R, Young JD: Functional substance P receptors on a human astrocytoma cell line (U-373 MG). Brain Res 488:328-331, 1989
66. Eistetter HR, Mills A, Brewster R, Alouani S, Rambosson C, Kawashima E: Functional characterization of neurokinin-1 receptors on human U373MG astrocytoma cells. Glia 6:89-95, 1992
67. Bang R, Sass G, Kiemer AK, Vollmar AM, Neuhuber WL, Tiegs G: 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, 2003
68. Rupniak NM, Carlson E, Boyce S, Webb JK, Hill RG: Enantioselective inhibition of the formalin paw late phase by the NK1 receptor antagonist L-733,060 in gerbils. Pain 67:189-195, 1996
69. Muñoz M, Rosso M, Coveñas R, Soult JA. Antitumoural action of neurokinin-1 receptor antagonists on human brain cancer cell lines. In: Brain Cancer: Therapy and Surgical Interventions 2006 (in press)
70. Lang K, Drell TL, Lindecke A, Niggemann B, Kaltschmidt C, Zaenker KS, Entschladen F: Induction of a metastatogenic tumor cell type by neurotransmitters and its pharmacological inhibition by established drugs. Int J Cancer 112:231-238, 2004
71. 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 USA 35:1859-1863, 1998
72. Langdon S, Sethi T, Richie A, Muir M, Smyth J, Rozengurt E: Broad spectrum neuropeptide antagonists inhibit the growth of small cell lung cancer in vivo. Cancer Res 52:4554-4557, 1992
73. 11] Substance P induces apoptosis in lung cancer cell lines in vitro. Biochem Bioph Res Com 199:1313-1319, 1994
74. 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, 1997
75. Palma C, Bigioni M, Irrissuto C, Nardelli F, Maggi CA, Manzini S: Anti-tumour activity of tachykinin NK1 receptor antagonists on human glioma U373 MG xenograft. Br J Cancer 82:480-487, 2000
76. Varty GB, Cohen-Williams ME, Hunter JC: The antidepressant-like effects of neurokinin NK1 receptor antagonists in a gerbil tail suspension test. Behav Pharmacol 14:87-95, 2003
77. Bang R, Biburger M, Neuhuber WL, Tiegs G: Neurokinin-1 Receptor antagonists protect mice from CD95- and tumor necrosis factor-α-mediated apoptotic. Liver Damage. J Pharmacol Exp Ther 308: 1174-1180, 2004
78. Goso C, Potier E, Manzini S, Szallasi A: Comparison of tachykinin NK1 receptors in human IM9 and U373 MG cells, using antagonist (FK888, (+/-)-CP-96,345, and RP 67580) binding. Eur J Pharmacol 254:221-227, 1994
79. Bringold F, Serrano M: Tumor suppressors and oncogenes in cellular senescence. Exp Gerontol 35: 317-329, 2000
80. Bulavin DV, Demidov ON, Saito S, Kauraniemi P, Phillips C, Amundson SA, Ambrosino C, Sauter G, Nebreda AR, Anderson CW, Kallioniemi A, Fornace AJ Jr, Appella E: Amplification of PPM1D in human tumors abrogates p53 tumor-suppressor activity. Nat Genet 31: 210-215, 2002
81. Ferbeyre GE, de Stanchina AW, Lin E, Querido ME, McCurrach GJ, Hannon S, Lowe SW: Oncogenic ras and p53 cooperate to induce cellular senescence. Mol Cell Biol 22: 3497-3508, 2002
82. Lin AW, Lowe SW: Oncogenic ras activates the ARF-p53 pathway to suppress epithelial cell transformation. Proc Natl Acad Sci USA 98:5025-5030, 2001
83. Serrano MA, Lin W, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602, 1997
84. Trost TM, Lausch EU, Fees SA, Schmitt S, Enklaar T, Reutzel D, Brixel LR, Schmidtke P, Maringer M, Schiffer IB, Heimerdinger CK, Hengstler JG, Fritz G, Bockamp EO, Prawitt D, Zabel BU, Spangenberg C: Premature senescence is a primary fail-safe mechanism of ERBB2-driven tumorigenesis in breast carcinoma cells. Cancer Res 65(3): 840-849, 2005
85. Collado M, Gil J, Efeyan A, Guerra C, Schuhmacher AJ, Barradas M, Benguria A, Zaballos A, Flores JM, Barbacid M, Beach D, Serrano M: Tumour biology: senescence in premalignant tumours. Nature 436(7051): 642, 2005
86. Braig M, Lee S, Loddenkemper C, Rudolph C, Peters AH, Schlegelberger B, Stein H, Dorken B, Jenuwein T, Schmitt CA: Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 436(7051): 660-665, 2005.
87. Comment in: Nature 436(7051):636-637, 2005
88. Ding HF, Fisher DE: Induction of apoptosis in cancer: new therapeutic opportunities. Ann Med 34(6): 451-469, 2002
89. Hennig IM, Laissue JA, Horisberger U, Reubi JC: Substance-P receptors in human primary neoplasms: tumoral and vascular localization.Int J Cancer 61:786-792, 1995
90. Seegers HC, Hood VC, Kidd BL, Cruwys SC, Walsh DA: Enhancement of angiogenesis by endogenous substance P release and neurokinin-1 receptors during neurogenic inflammation. J Pharmacol Exp Ther 306(1): 8-12, 2003
91. Jacobs CM, Boldingh KA, Slagsvold HH, Thoresen GH, Paulsen RE: ERK2 prohibits apoptosis-induced subcellular translocation of orphan nuclear receptor NGFI-B/TR3. Biol Chem 279: 50097-50101, 2004
92. Castro-Obregon S, Rao SV, del Rio G, Chen SF, Poksay KS, Rabizadeh S, Vesce S, Zhang XK, Swanson RA, Bredesen DE: Alternative, nonapoptotic programmed cell death. Mediation By Arrestin 2, Erk2, And Nur77. J Biol Chem 279:17543-17553, 2004
93. Kramer MS, Cutler N, Feighner J, Shrivastava R, Carman J, Sramek JJ, Reines SA, Liu G, Snavely D, Wyatt-Knowles E, Hale JJ, Mills SG, MacCoss M, Swain CJ, Harrison T, Hill RG, Hefti F, Scolnick EM, Cascieri MA, Chicchi GG, Sadowski S, Williams AR, Hewson L, Smith D, Carlson EJ, Hargreaves RJ, Rupniak NM: Distinct mechanism for antidepressant activity by blockade of central substance P receptors. Science 281:1640-1645, 1998