Truncated neurokinin-1 receptor is increased in colonic epithelial cells from patients with colitis-associated cancer

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 42, 2011, Pages 17420-17425

  Gillespie, Earl ^a   Leeman, Susan E ^a   Watts, Luisa A ^a   Coukos, Jennifer A ^a   O'Brien, Michael J ^a   Cerda, Sandra R ^a   Farraye, Francis A ^a   Stucchi, Arthur F ^a   Becker, James M ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Colon cancer; IBD; Receptor splice variants; Substance P

Indexed keywords

MESSENGER RNA; NEUROKININ 1 RECEPTOR;

ARTICLE; COLON CANCER; COLON CARCINOMA; COMPARATIVE STUDY; EPITHELIUM CELL; GASTROINTESTINAL DYSPLASIA; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; ULCERATIVE COLITIS;

ALTERNATIVE SPLICING; CELL TRANSFORMATION, NEOPLASTIC; COLITIS, ULCERATIVE; COLON; COLORECTAL NEOPLASMS; HUMANS; INTESTINAL MUCOSA; LIGANDS; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; RECEPTORS, NEUROKININ-1; RNA, MESSENGER; RNA, NEOPLASM; SUBSTANCE P;

EID: 80054798925     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1114275108     Document Type: Article

References (49)

1. O'Connor PM, Lapointe TK, Beck PL, Buret AG (2010) Mechanisms by which inflammation may increase intestinal cancer risk in inflammatory bowel disease. Inflamm Bowel Dis 16:1411-1420.
2. Farraye FA, et al. (2010) AGA medical position statement on the diagnosis and management of colorectal neoplasia in inflammatory bowel disease. Gastroenterology 138:738-745.
3. Ekbom A, Helmick C, Zack M, Adami HO (1990) Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med 323:1228-1233. (Pubitemid 20366527)
4. Eaden JA, Abrams KR, Mayberry JF (2001) The risk of colorectal cancer in ulcerative colitis: A meta-analysis. Gut 48:526-535. (Pubitemid 32234798)
5. von Euler US, Gaddum JH (1931) An unidentified depressor substance in certain tissue extracts. J Physiol 72:74-87.
6. Chang MM, Leeman SE (1970) Isolation of a sialogogic peptide from bovine hypothalamic tissue and its characterization as substance P. J Biol Chem 245:4784-4790.
7. Ho WZ, Lai JP, Zhu XH, Uvaydova M, Douglas SD (1997) Human monocytes and macrophages express substance P and neurokinin-1 receptor. J Immunol 159:5654-5660. (Pubitemid 127470097)
8. Quartara L, Maggi CA (1998) The tachykinin NK1 receptor. Part II: Distribution and pathophysiological roles. Neuropeptides 32:1-49. (Pubitemid 28167857)
9. Stucchi AF, et al. (2003) A neurokinin 1 receptor antagonist reduces an ongoing ileal pouch inflammation and the response to a subsequent inflammatory stimulus. Am J Physiol Gastrointest Liver Physiol 285:G1259-G1267. (Pubitemid 37449014)
10. Pothoulakis C, et al. (1998) Substance P receptor expression in intestinal epithelium in clostridium difficile toxin A enteritis in rats. Am J Physiol 275:G68-G75.
11. Goode T, et al. (2000) Neurokinin-1 receptor expression in inflammatory bowel disease: Molecular quantitation and localisation. Gut 47:387-396.
12. Renzi D, Pellegrini B, Tonelli F, Surrenti C, Calabrò A (2000) Substance P (neurokinin-1) and neurokinin A (neurokinin-2) receptor gene and protein expression in the healthy and inflamed human intestine. Am J Pathol 157:1511-1522.
13. Michalski CW, et al. (2007) Increase in substance P precursor mRNA in noninflamed small-bowel sections in patients with Crohn's disease. Am J Surg 193:476-481. (Pubitemid 46412240)
14. ter Beek WP, Biemond I, Muller ES, van den Berg M, Lamers CB (2007) Substance P receptor expression in patients with inflammatory bowel disease. Determination by three different techniques, i.e., storage phosphor autoradiography, RT-PCR and immunohistochemistry. Neuropeptides 41:301-306. (Pubitemid 47247865)
15. Muñoz M, et al. (2010) The NK-1 receptor is expressed in human melanoma and is involved in the antitumor action of the NK-1 receptor antagonist aprepitant on melanoma cell lines. Lab Invest 90:1259-1269.
16. Esteban F, et al. (2009) Expression of substance P and neurokinin-1-receptor in laryngeal cancer: Linking chronic inflammation to cancer promotion and progression. Histopathology 54:258-260.
17. Rosso M, Robles-Frías MJ, Coveñas R, Salinas-Martín MV, Muñoz M (2008) The NK-1 receptor is expressed in human primary gastric and colon adenocarcinomas and is involved in the antitumor action of L-733,060 and the mitogenic action of substance P on human gastrointestinal cancer cell lines. Tumour Biol 29:245-254.
18. 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.
19. Schulz S, Stumm R, Röcken C, Mawrin C, Schulz S (2006) Immunolocalization of full-length NK1 tachykinin receptors in human tumors. J Histochem Cytochem 54: 1015-1020. (Pubitemid 44298588)
20. Muñoz M, et al. (2008) NK-1 receptor antagonists induce apoptosis and counteract substance P-related mitogenesis in human laryngeal cancer cell line HEp-2. Invest New Drugs 26:111-118.
21. Pagán B, et al. (2010) Effect of a neurokinin-1 receptor antagonist in a rat model of colitis-associated colon cancer. Anticancer Res 30:3345-3353.
22. Kage R, Leeman SE, Boyd ND (1993) Biochemical characterization of two different forms of the substance P receptor in rat submaxillary gland. J Neurochem 60:347-351. (Pubitemid 23006737)
23. Fong TM, Anderson SA, Yu H, Huang RR, Strader CD (1992) Differential activation of intracellular effector by two isoforms of human neurokinin-1 receptor. Mol Pharmacol 41:24-30.
24. Ramkissoon SH, Patel PS, Taborga M, Rameshwar P (2007) Nuclear factor-kappaB is central to the expression of truncated neurokinin-1 receptor in breast cancer: Implication for breast cancer cell quiescence within bone marrow stroma. Cancer Res 67:1653-1659. (Pubitemid 46383391)
25. Patel HJ, Ramkissoon SH, Patel PS, Rameshwar P (2005) Transformation of breast cells by truncated neurokinin-1 receptor is secondary to activation by preprotachykinin-A peptides. Proc Natl Acad Sci USA 102:17436-17441. (Pubitemid 41740884)
26. Lai JP, et al. (2008) Differences in the length of the carboxyl terminus mediate functional properties of neurokinin-1 receptor. Proc Natl Acad Sci USA 105:12605-12610.
27. Li H, et al. (1997) A substance P (neurokinin-1) receptor mutant carboxyl-terminally truncated to resemble a naturally occurring receptor isoform displays enhanced responsiveness and resistance to desensitization. Proc Natl Acad Sci USA 94:9475-9480. (Pubitemid 27357854)
28. Déry O, Defea KA, Bunnett NW (2001) Protein kinase C-mediated desensitization of the neurokinin 1 receptor. Am J Physiol Cell Physiol 280:C1097-C1106.
29. Morteau O, Lu B, Gerard C, Gerard NP (2001) Hemokinin 1 is a full agonist at the substance P receptor. Nat Immunol 2:1088. (Pubitemid 33130136)
30. Bellucci F, et al. (2002) Pharmacological profile of the novel mammalian tachykinin, hemokinin 1. Br J Pharmacol 135:266-274. (Pubitemid 34102121)
31. Maggi CA (1995) The mammalian tachykinin receptors. Gen Pharmacol 26:911-944.
32. González Moles MA, et al. (2009) A role for the substance P/NK-1 receptor complex in cell proliferation and apoptosis in oral lichen planus. Oral Dis 15:162-169.
33. Donnerer J, Schuligoi R, Stein C (1992) Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: Evidence for a regulatory function of nerve growth factor in vivo. Neuroscience 49:693-698.
34. Keränen U, et al. (1995) Changes in substance P-immunoreactive innervation of human colon associated with ulcerative colitis. Dig Dis Sci 40:2250-2258.
35. Choy MY, Walker-Smith JA, Williams CB, MacDonald TT (1990) Differential expression of CD25 (interleukin-2 receptor) on lamina propria T cells and macrophages in the intestinal lesions in Crohn's disease and ulcerative colitis. Gut 31:1365-1370.
36. Liu L, et al. (2011) Distinct differences in tachykinin gene expression in ulcerative colitis, Crohn's disease and diverticular disease: A role for hemokinin-1? Neurogastroenterol Motil 23:475-483.
37. Rogler G, et al. (1998) Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology 115:357-369. (Pubitemid 28363428)
38. Reed KL, et al. (2005) NF-kappaB activation precedes increases in mRNA encoding neurokinin-1 receptor, proinflammatory cytokines, and adhesion molecules in dextran sulfate sodium-induced colitis in rats. Dig Dis Sci 50:2366-2378. (Pubitemid 43106398)
39. Karhausen J, et al. (2004) Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J Clin Invest 114:1098-1106. (Pubitemid 39578699)
40. Giatromanolaki A, et al. (2003) Hypoxia inducible factor 1alpha and 2alpha overexpression in inflammatory bowel disease. J Clin Pathol 56:209-213. (Pubitemid 36308037)
41. Okuda T, et al. (2006) Hypoxia-inducible factor-1 alpha and vascular endothelial growth factor expression in ischaemic colitis and ulcerative colitis. Aliment Pharmacol Ther 24(Suppl 4):182-188.
42. Ryan S, Taylor CT, McNicholas WT (2005) Selective activation of inflammatory pathways by intermittent hypoxia in obstructive sleep apnea syndrome. Circulation 112:2660-2667. (Pubitemid 41532603)
43. Cummins EP, et al. (2006) Prolyl hydroxylase-1 negatively regulates IkappaB kinase-β, giving insight into hypoxia-induced NFkappaB activity. Proc Natl Acad Sci USA 103: 18154-18159. (Pubitemid 44871628)
44. Turpin E, et al. (1999) Stress-induced aberrant splicing of TSG101: Association to high tumor grade and p53 status in breast cancers. Oncogene 18:7834-7837. (Pubitemid 30052768)
45. Körner M, Miller LJ (2009) Alternative splicing of pre-mRNA in cancer: Focus on G protein-coupled peptide hormone receptors. Am J Pathol 175:461-472.
46. Sveen A, et al. (2011) Transcriptome instability in colorectal cancer identified by exon microarray analyses: Associations with splicing factor expression levels and patient survival. Genome Med 3:32.
47. Pagedar NA, et al. (2006) Gene expression analysis of distinct populations of cells isolated from mouse and human inner ear FFPE tissue using laser capture microdissection - a technical report based on preliminary findings. Brain Res 1091:289-299. (Pubitemid 43993885)
48. Nonn L, Vaishnav A, Gallagher L, Gann PH (2010) mRNA and micro-RNA expression analysis in laser-capture microdissected prostate biopsies: Valuable tool for risk assessment and prevention trials. Exp Mol Pathol 88:45-51.
49. Bremer AA, Leeman SE (2010) Substance P. eLS (Wiley, New York).