Skip to main content
Top
Published in: Current Treatment Options in Oncology 1/2020

Open Access 01-01-2020 | Metastasis | Lower Gastrointestinal Cancers (AB Benson, Section Editor)

Opioids in Cancer Development, Progression and Metastasis: Focus on Colorectal Cancer

Authors: Adrian Szczepaniak, Jakub Fichna, PhD, DSc, Marta Zielińska, PhD

Published in: Current Treatment Options in Oncology | Issue 1/2020

Login to get access

Opinion statement

So far, opioids have been successfully used to reduce cancer pain in patients in order to improve their quality of life. However, the use of opioids leads to numerous side effects such as constipation, drowsiness, nausea, itching, increased sweating and hormonal changes. In this review, we described the action of opioids in several molecular pathways significant for maintenance of the intestinal homeostasis including the impact on the intestinal epithelium integrity, changes in microbiome composition, modulation of the immune system or induction of apoptosis and inhibition of angiogenesis. We summed up the role of individual opioids in the processes involved in the growth and development of cancer and elucidated if targeting opioid receptors may constitute novel therapeutic option in colon cancer.
Literature
1.
go back to reference • Fitzmaurice C, Allen C, Barber RM, Barregard L, Bhutta ZA, Brenner H, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 32 cancer groups, 1990 to 2015: a systematic analysis for the Global Burden of Disease Study. JAMA Oncol. 2017;3(4):524–48 It is a comprehensive analysis (performed using Global Burden of Disease methodology) of mortality, incidence, years lived with disability, years of life lost, and disability-adjusted life-years for 32 cancers in 195 countries and territories from 1990 to 2015. • Fitzmaurice C, Allen C, Barber RM, Barregard L, Bhutta ZA, Brenner H, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 32 cancer groups, 1990 to 2015: a systematic analysis for the Global Burden of Disease Study. JAMA Oncol. 2017;3(4):524–48 It is a comprehensive analysis (performed using Global Burden of Disease methodology) of mortality, incidence, years lived with disability, years of life lost, and disability-adjusted life-years for 32 cancers in 195 countries and territories from 1990 to 2015.
4.
go back to reference Mishra J, Drummond J, Quazi SH, Karanki SS, Shaw JJ, Chen B, et al. Prospective of colon cancer treatments and scope for combinatorial approach to enhanced cancer cell apoptosis. Crit Rev Oncol Hematol. 2013:232–50.PubMed Mishra J, Drummond J, Quazi SH, Karanki SS, Shaw JJ, Chen B, et al. Prospective of colon cancer treatments and scope for combinatorial approach to enhanced cancer cell apoptosis. Crit Rev Oncol Hematol. 2013:232–50.PubMed
5.
go back to reference Zagon IS, Verderame MF, McLaughlin PJ. The biology of the opioid growth factor receptor (OGFr). Brain Res Brain Res Rev. 2002;38(3):351–76.PubMed Zagon IS, Verderame MF, McLaughlin PJ. The biology of the opioid growth factor receptor (OGFr). Brain Res Brain Res Rev. 2002;38(3):351–76.PubMed
6.
go back to reference Gach K, Szemraj J, Stasikowska-Kanicka O, Danilewicz M, Janecka A. Opioid-receptor gene expression and localization in cancer cells. Open Life Sci. 2011;6(1):10–5. Gach K, Szemraj J, Stasikowska-Kanicka O, Danilewicz M, Janecka A. Opioid-receptor gene expression and localization in cancer cells. Open Life Sci. 2011;6(1):10–5.
7.
go back to reference • Boland JW, McWilliams K, Ahmedzai SH, Pockley AG. Effects of opioids on immunologic parameters that are relevant to anti-tumour immune potential in patients with cancer: a systematic literature review. Br J Cancer. 2014:866–73 This interesting review summed up a knowledge about impact of different opioids on anti-tumour immunity and it can be found how difficult is to manage with drug therapy using opioids in patients with cancer.PubMedPubMedCentral • Boland JW, McWilliams K, Ahmedzai SH, Pockley AG. Effects of opioids on immunologic parameters that are relevant to anti-tumour immune potential in patients with cancer: a systematic literature review. Br J Cancer. 2014:866–73 This interesting review summed up a knowledge about impact of different opioids on anti-tumour immunity and it can be found how difficult is to manage with drug therapy using opioids in patients with cancer.PubMedPubMedCentral
8.
go back to reference Maneckjee R. Anticancer effects of therapeutic opioids. Pain Forum. 1999;8(4):213–5. Maneckjee R. Anticancer effects of therapeutic opioids. Pain Forum. 1999;8(4):213–5.
9.
go back to reference Akbari M, Naghibzadeh-Tahami A, Khanjani N, Baneshi MR, Kamali E, Hesampour M, et al. Opium as a risk factor for bladder cancer: a population-based case-control study in Iran. Arch Iran Med. 2015;18(9):567–71.PubMed Akbari M, Naghibzadeh-Tahami A, Khanjani N, Baneshi MR, Kamali E, Hesampour M, et al. Opium as a risk factor for bladder cancer: a population-based case-control study in Iran. Arch Iran Med. 2015;18(9):567–71.PubMed
10.
go back to reference Shakeri R, Malekzadeh R, Etemadi A, Nasrollahzadeh D, Aghcheli K, Sotoudeh M, et al. Opium: an emerging risk factor for gastric adenocarcinoma. Int J Cancer. 2013;133(2):455–61.PubMed Shakeri R, Malekzadeh R, Etemadi A, Nasrollahzadeh D, Aghcheli K, Sotoudeh M, et al. Opium: an emerging risk factor for gastric adenocarcinoma. Int J Cancer. 2013;133(2):455–61.PubMed
11.
go back to reference Razmpa E, Saedi B, Motiee-Langroudi M, Garajei A, Hoseinpor S, Motamedi MHK. Opium usage as an etiologic factor of oral cavity cancer. J Craniofac Surg. 2014;25(5):e505–7.PubMed Razmpa E, Saedi B, Motiee-Langroudi M, Garajei A, Hoseinpor S, Motamedi MHK. Opium usage as an etiologic factor of oral cavity cancer. J Craniofac Surg. 2014;25(5):e505–7.PubMed
12.
go back to reference Shakeri R, Kamangar F, Nasrollahzadeh D, Nouraie M, Khademi H, Etemadi A, et al. Is opium a real risk factor for esophageal cancer or just a methodological artifact? hospital and neighborhood controls in case-control studies. PLoS One. 2012;7(3):e32711.PubMedPubMedCentral Shakeri R, Kamangar F, Nasrollahzadeh D, Nouraie M, Khademi H, Etemadi A, et al. Is opium a real risk factor for esophageal cancer or just a methodological artifact? hospital and neighborhood controls in case-control studies. PLoS One. 2012;7(3):e32711.PubMedPubMedCentral
13.
go back to reference Frenklakh L, Bhat RS, Bhaskaran M, Sharma S, Sharma M, Dinda A, et al. Morphine-induced degradation of the host defense barrier. Dig Dis Sci. 2006;51(2):318–25.PubMed Frenklakh L, Bhat RS, Bhaskaran M, Sharma S, Sharma M, Dinda A, et al. Morphine-induced degradation of the host defense barrier. Dig Dis Sci. 2006;51(2):318–25.PubMed
14.
go back to reference Harari Y, Weisbrodt NW, Moody FG. The effect of morphine on mast cell-mediated mucosal permeability. Surgery. 2006;139(1):54–60.PubMed Harari Y, Weisbrodt NW, Moody FG. The effect of morphine on mast cell-mediated mucosal permeability. Surgery. 2006;139(1):54–60.PubMed
16.
go back to reference Pasz-Walczak G, Kordek R, Faflik M. P21 (WAF1) expression in colorectal cancer: correlation with P53 and cyclin D1 expression, clinicopathological parameters and prognosis. Pathol Res Pract. 2001;197(10):683–9.PubMed Pasz-Walczak G, Kordek R, Faflik M. P21 (WAF1) expression in colorectal cancer: correlation with P53 and cyclin D1 expression, clinicopathological parameters and prognosis. Pathol Res Pract. 2001;197(10):683–9.PubMed
17.
go back to reference • Chelakkot C, Ghim J, Ryu SH. Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp Mol Med. 2018;50(8) An interesting review on the intestinal epithelial barrier. • Chelakkot C, Ghim J, Ryu SH. Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp Mol Med. 2018;50(8) An interesting review on the intestinal epithelial barrier.
18.
go back to reference Wang F, Roy S. Gut homeostasis, microbial dysbiosis, and opioids. Toxicol Pathol. 2017;45(1):150–6.PubMed Wang F, Roy S. Gut homeostasis, microbial dysbiosis, and opioids. Toxicol Pathol. 2017;45(1):150–6.PubMed
19.
go back to reference Mahajan SD, Aalinkeel R, Sykes DE, Reynolds JL, Bindukumar B, Fernandez SF, et al. Tight junction regulation by morphine and HIV-1 tat modulates blood–brain barrier permeability. J Clin Immunol. 2008;28(5):528–41.PubMed Mahajan SD, Aalinkeel R, Sykes DE, Reynolds JL, Bindukumar B, Fernandez SF, et al. Tight junction regulation by morphine and HIV-1 tat modulates blood–brain barrier permeability. J Clin Immunol. 2008;28(5):528–41.PubMed
20.
go back to reference Meng J, Yu H, Ma J, Wang J, Banerjee S, Charboneau R, et al. Morphine induces bacterial translocation in mice by compromising intestinal barrier function in a TLR-dependent manner. Buch SJ, editor. PLoS One. 2013;8(1):e54040.PubMedPubMedCentral Meng J, Yu H, Ma J, Wang J, Banerjee S, Charboneau R, et al. Morphine induces bacterial translocation in mice by compromising intestinal barrier function in a TLR-dependent manner. Buch SJ, editor. PLoS One. 2013;8(1):e54040.PubMedPubMedCentral
21.
go back to reference •• Bauman BD, Meng J, Zhang L, Louiselle A, Zheng E, Banerjee S, et al. Enteric glial-mediated enhancement of intestinal barrier integrity is compromised by morphine. J Surg Res. 2017;219:214–21 An important involvement of the maintenance of intestinal epithelium integrity.PubMedPubMedCentral •• Bauman BD, Meng J, Zhang L, Louiselle A, Zheng E, Banerjee S, et al. Enteric glial-mediated enhancement of intestinal barrier integrity is compromised by morphine. J Surg Res. 2017;219:214–21 An important involvement of the maintenance of intestinal epithelium integrity.PubMedPubMedCentral
22.
go back to reference Okura T, Ozawa T, Ibe M, Taki Y, Kimura M, Kagawa Y, et al. Effects of repeated morphine treatment on the antinociceptive effects, intestinal absorption, and efflux from intestinal epithelial cells of morphine. Biol Pharm Bull. 2009;32(9):1571–5.PubMed Okura T, Ozawa T, Ibe M, Taki Y, Kimura M, Kagawa Y, et al. Effects of repeated morphine treatment on the antinociceptive effects, intestinal absorption, and efflux from intestinal epithelial cells of morphine. Biol Pharm Bull. 2009;32(9):1571–5.PubMed
23.
go back to reference •• Wang F, Meng J, Zhang L, Johnson T, Chen C, Roy S. Morphine induces changes in the gut microbiome and metabolome in a morphine dependence model. Sci Rep. 2018;8(1):3596 In this paper authors indicated that morphine induced distinct alterations in the gut microbiome and metabolome, contributed to negative consequences combined with opioid administration.PubMedPubMedCentral •• Wang F, Meng J, Zhang L, Johnson T, Chen C, Roy S. Morphine induces changes in the gut microbiome and metabolome in a morphine dependence model. Sci Rep. 2018;8(1):3596 In this paper authors indicated that morphine induced distinct alterations in the gut microbiome and metabolome, contributed to negative consequences combined with opioid administration.PubMedPubMedCentral
24.
go back to reference de Almeida CV, Taddei A, Amedei A. The controversial role of enterococcus faecalis in colorectal cancer. Ther Adv Gastroenterol. 2018;11:1756284818783606. de Almeida CV, Taddei A, Amedei A. The controversial role of enterococcus faecalis in colorectal cancer. Ther Adv Gastroenterol. 2018;11:1756284818783606.
25.
go back to reference Huycke MM, Abrams V, Moore DR. Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA. Carcinogenesis. 2002;23(3):529–36.PubMed Huycke MM, Abrams V, Moore DR. Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA. Carcinogenesis. 2002;23(3):529–36.PubMed
26.
go back to reference Ahn J, Sinha R, Pei Z, Dominianni C, Wu J, Shi J, et al. Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst. 2013;105(24):1907–11.PubMedPubMedCentral Ahn J, Sinha R, Pei Z, Dominianni C, Wu J, Shi J, et al. Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst. 2013;105(24):1907–11.PubMedPubMedCentral
27.
go back to reference Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012;22(2):299–306.PubMedPubMedCentral Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012;22(2):299–306.PubMedPubMedCentral
28.
go back to reference Greiner T, Bäckhed F. Effects of the gut microbiota on obesity and glucose homeostasis. Trends Endocrinol Metab. 2011;22(4):117–23.PubMed Greiner T, Bäckhed F. Effects of the gut microbiota on obesity and glucose homeostasis. Trends Endocrinol Metab. 2011;22(4):117–23.PubMed
29.
30.
go back to reference Liang X, Liu R, Chen C, Ji F, Li T. Opioid system modulates the immune function: a review. Transl Perioper Pain Med. 2016;1(1):5–13.PubMedPubMedCentral Liang X, Liu R, Chen C, Ji F, Li T. Opioid system modulates the immune function: a review. Transl Perioper Pain Med. 2016;1(1):5–13.PubMedPubMedCentral
31.
go back to reference Baldini A, Von Korff M, Lin EHB. A review of potential adverse effects of long-term opioid therapy: a practitioner’s guide. Prim Care Companion CNS Disord. 2012;14(3). Baldini A, Von Korff M, Lin EHB. A review of potential adverse effects of long-term opioid therapy: a practitioner’s guide. Prim Care Companion CNS Disord. 2012;14(3).
32.
go back to reference Chan Y-Y, Yang S-N, Lin J-C, Chang J-L, Lin J-G, Lo W-Y. Inflammatory response in heroin addicts undergoing methadone maintenance treatment. Psychiatry Res. 2015;226(1):230–4.PubMed Chan Y-Y, Yang S-N, Lin J-C, Chang J-L, Lin J-G, Lo W-Y. Inflammatory response in heroin addicts undergoing methadone maintenance treatment. Psychiatry Res. 2015;226(1):230–4.PubMed
33.
go back to reference • Fakhraei N, Javadian N, Rahimian R, Nili F, Rahimi N, Hashemizadeh S, et al. Involvement of central opioid receptors in protective effects of methadone on experimental colitis in rats. Inflammopharmacology. 2018;26(6):1399–413 In this study it was found that methadone may induce anti-inflammatory action during colonic inflammation through opioid receptors located mainly in the central nervous system.PubMed • Fakhraei N, Javadian N, Rahimian R, Nili F, Rahimi N, Hashemizadeh S, et al. Involvement of central opioid receptors in protective effects of methadone on experimental colitis in rats. Inflammopharmacology. 2018;26(6):1399–413 In this study it was found that methadone may induce anti-inflammatory action during colonic inflammation through opioid receptors located mainly in the central nervous system.PubMed
34.
go back to reference Du J-Y, Liang Y, Fang J-F, Jiang Y-L, Shao X-M, He X-F, et al. Effect of systemic injection of heterogenous and homogenous opioids on peripheral cellular immune response in rats with bone cancer pain: a comparative study. Exp Ther Med. 2016;12(4):2568–76.PubMedPubMedCentral Du J-Y, Liang Y, Fang J-F, Jiang Y-L, Shao X-M, He X-F, et al. Effect of systemic injection of heterogenous and homogenous opioids on peripheral cellular immune response in rats with bone cancer pain: a comparative study. Exp Ther Med. 2016;12(4):2568–76.PubMedPubMedCentral
35.
go back to reference Weerts EM, Kim YK, Wand GS, Dannals RF, Lee JS, Frost JJ, et al. Differences in δ- and μ-opioid receptor blockade measured by positron emission tomography in naltrexone-treated recently abstinent alcohol-dependent subjects. Neuropsychopharmacology. 2008;33(3):653–65.PubMed Weerts EM, Kim YK, Wand GS, Dannals RF, Lee JS, Frost JJ, et al. Differences in δ- and μ-opioid receptor blockade measured by positron emission tomography in naltrexone-treated recently abstinent alcohol-dependent subjects. Neuropsychopharmacology. 2008;33(3):653–65.PubMed
36.
go back to reference Lee JD, Friedmann PD, Kinlock TW, Nunes EV, Boney TY, Hoskinson RA, et al. Extended-release naltrexone to prevent opioid relapse in criminal justice offenders. N Engl J Med. 2016;374(13):1232–42.PubMedPubMedCentral Lee JD, Friedmann PD, Kinlock TW, Nunes EV, Boney TY, Hoskinson RA, et al. Extended-release naltrexone to prevent opioid relapse in criminal justice offenders. N Engl J Med. 2016;374(13):1232–42.PubMedPubMedCentral
37.
go back to reference Yi Z, Guo S, Hu X, Wang X, Zhang X, Griffin N, et al. Functional modulation on macrophage by low dose naltrexone (LDN). Int Immunopharmacol. 2016;39:397–402.PubMed Yi Z, Guo S, Hu X, Wang X, Zhang X, Griffin N, et al. Functional modulation on macrophage by low dose naltrexone (LDN). Int Immunopharmacol. 2016;39:397–402.PubMed
38.
go back to reference Kajihara M, Takakura K, Kanai T, Ito Z, Saito K, Takami S, et al. Dendritic cell-based cancer immunotherapy for colorectal cancer. World J Gastroenterol. 2016;22(17):4275–86.PubMedPubMedCentral Kajihara M, Takakura K, Kanai T, Ito Z, Saito K, Takami S, et al. Dendritic cell-based cancer immunotherapy for colorectal cancer. World J Gastroenterol. 2016;22(17):4275–86.PubMedPubMedCentral
39.
go back to reference Liu J, Chen W, Meng J, Lu C, Wang E, Shan F, et al. Induction on differentiation and modulation of bone marrow progenitor of dendritic cell by methionine enkephalin (MENK). Cancer Immunol Immunother. 2012;61(10):1699–711.PubMed Liu J, Chen W, Meng J, Lu C, Wang E, Shan F, et al. Induction on differentiation and modulation of bone marrow progenitor of dendritic cell by methionine enkephalin (MENK). Cancer Immunol Immunother. 2012;61(10):1699–711.PubMed
40.
go back to reference Beilin B, Shavit Y, Hart J, Mordashov B, Cohn S, Notti I, et al. Effects of anesthesia based on large versus small doses of fentanyl on natural killer cell cytotoxicity in the perioperative period. Anesth Analg. 1996;82(3):492–7.PubMed Beilin B, Shavit Y, Hart J, Mordashov B, Cohn S, Notti I, et al. Effects of anesthesia based on large versus small doses of fentanyl on natural killer cell cytotoxicity in the perioperative period. Anesth Analg. 1996;82(3):492–7.PubMed
41.
go back to reference Yeager MP, Procopio MA, DeLeo JA, Arruda JL, Hildebrandt L, Howell AL. Intravenous fentanyl increases natural killer cell cytotoxicity and circulating CD16(+) lymphocytes in humans. Anesth Analg. 2002;94(1):94–9.PubMed Yeager MP, Procopio MA, DeLeo JA, Arruda JL, Hildebrandt L, Howell AL. Intravenous fentanyl increases natural killer cell cytotoxicity and circulating CD16(+) lymphocytes in humans. Anesth Analg. 2002;94(1):94–9.PubMed
42.
go back to reference Odunayo A, Dodam JR, Kerl ME, DeClue AE. Immunomodulatory effects of opioids. J Vet Emerg Crit Care. 2010. Odunayo A, Dodam JR, Kerl ME, DeClue AE. Immunomodulatory effects of opioids. J Vet Emerg Crit Care. 2010.
43.
go back to reference Palm S, Lehzen S, Mignat C, Steinmann J, Leimenstoll G, Maier C. Does prolonged oral treatment with sustained-release morphine tablets influence immune function? Anesth Analg. 1998;86(1):166–72.PubMed Palm S, Lehzen S, Mignat C, Steinmann J, Leimenstoll G, Maier C. Does prolonged oral treatment with sustained-release morphine tablets influence immune function? Anesth Analg. 1998;86(1):166–72.PubMed
44.
go back to reference Makimura C, Arao T, Matsuoka H, Takeda M, Kiyota H, Tsurutani J, et al. Prospective study evaluating the plasma concentrations of twenty-six cytokines and response to morphine treatment in cancer patients. Anticancer Res. 2011;31(12):4561–8.PubMed Makimura C, Arao T, Matsuoka H, Takeda M, Kiyota H, Tsurutani J, et al. Prospective study evaluating the plasma concentrations of twenty-six cytokines and response to morphine treatment in cancer patients. Anticancer Res. 2011;31(12):4561–8.PubMed
45.
go back to reference Suzuki M, Sakurada T, Gotoh K, Watanabe S, Satoh N. Correlation between the administration of morphine or oxycodone and the development of infections in patients with cancer pain. Am J Hosp Palliat Med. 2013;30(7):712–6. Suzuki M, Sakurada T, Gotoh K, Watanabe S, Satoh N. Correlation between the administration of morphine or oxycodone and the development of infections in patients with cancer pain. Am J Hosp Palliat Med. 2013;30(7):712–6.
46.
go back to reference Molina-Martínez LM, González-Espinosa C, Cruz SL. Dissociation of immunosuppressive and nociceptive effects of fentanyl, but not morphine, after repeated administration in mice: fentanyl-induced sensitization to LPS. Brain Behav Immun. 2014;42:60–4.PubMed Molina-Martínez LM, González-Espinosa C, Cruz SL. Dissociation of immunosuppressive and nociceptive effects of fentanyl, but not morphine, after repeated administration in mice: fentanyl-induced sensitization to LPS. Brain Behav Immun. 2014;42:60–4.PubMed
47.
go back to reference Franchi S, Panerai AE, Sacerdote P. Buprenorphine ameliorates the effect of surgery on hypothalamus–pituitary–adrenal axis, natural killer cell activity and metastatic colonization in rats in comparison with morphine or fentanyl treatment. Brain Behav Immun. 2007;21(6):767–74.PubMed Franchi S, Panerai AE, Sacerdote P. Buprenorphine ameliorates the effect of surgery on hypothalamus–pituitary–adrenal axis, natural killer cell activity and metastatic colonization in rats in comparison with morphine or fentanyl treatment. Brain Behav Immun. 2007;21(6):767–74.PubMed
48.
go back to reference Shavit Y, Ben-Eliyahu S, Zeidel A, Beilin B. Effects of fentanyl on natural killer cell activity and on resistance to tumor metastasis in rats. Neuroimmunomodulation. 2004;11(4):255–60.PubMed Shavit Y, Ben-Eliyahu S, Zeidel A, Beilin B. Effects of fentanyl on natural killer cell activity and on resistance to tumor metastasis in rats. Neuroimmunomodulation. 2004;11(4):255–60.PubMed
49.
go back to reference Goldar S, Khaniani MS, Derakhshan SM, Baradaran B. Molecular mechanisms of apoptosis and roles in cancer development and treatment. Asian Pac J Cancer Prev. 2015;16(6):2129–44.PubMed Goldar S, Khaniani MS, Derakhshan SM, Baradaran B. Molecular mechanisms of apoptosis and roles in cancer development and treatment. Asian Pac J Cancer Prev. 2015;16(6):2129–44.PubMed
50.
go back to reference Cory S, Huang DCS, Adams JM. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene. 2003;22(53):8590–607.PubMed Cory S, Huang DCS, Adams JM. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene. 2003;22(53):8590–607.PubMed
51.
go back to reference Tian M, Jin L, Li R, Zhu S, Ji M, Li W. Comparison of oxycodone and morphine on the proliferation, apoptosis and expression of related molecules in the A549 human lung adenocarcinoma cell line. Exp Ther Med. 2016;12(2):559–66.PubMedPubMedCentral Tian M, Jin L, Li R, Zhu S, Ji M, Li W. Comparison of oxycodone and morphine on the proliferation, apoptosis and expression of related molecules in the A549 human lung adenocarcinoma cell line. Exp Ther Med. 2016;12(2):559–66.PubMedPubMedCentral
52.
go back to reference Xu YJ, Li SY, Cheng Q, Chen WK, Wang SL, Ren Y, et al. Effects of anaesthesia on proliferation, invasion and apoptosis of LoVo colon cancer cells in vitro. Anaesthesia. 2016;71(2):147–54.PubMed Xu YJ, Li SY, Cheng Q, Chen WK, Wang SL, Ren Y, et al. Effects of anaesthesia on proliferation, invasion and apoptosis of LoVo colon cancer cells in vitro. Anaesthesia. 2016;71(2):147–54.PubMed
53.
go back to reference Tegeder I, Grösch S, Schmidtko A, Häussler A, Schmidt H, Niederberger E, et al. G protein-independent G1 cell cycle block and apoptosis with morphine in adenocarcinoma cells: involvement of p53 phosphorylation. Cancer Res. 2003;63(8):1846–52.PubMed Tegeder I, Grösch S, Schmidtko A, Häussler A, Schmidt H, Niederberger E, et al. G protein-independent G1 cell cycle block and apoptosis with morphine in adenocarcinoma cells: involvement of p53 phosphorylation. Cancer Res. 2003;63(8):1846–52.PubMed
54.
go back to reference Zagon IS, McLaughlin PJ. Opioids and the apoptotic pathway in human cancer cells. Neuropeptides. 2003;37(2):79–88.PubMed Zagon IS, McLaughlin PJ. Opioids and the apoptotic pathway in human cancer cells. Neuropeptides. 2003;37(2):79–88.PubMed
55.
go back to reference Kocak N, Ozen F, Yildirim IH, Duran Y. Fentanyl inhibits tumorigenesis from human breast stem cells by inducing apoptosis. Asian Pac J Cancer Prev. 2017;18(3):735–9.PubMedPubMedCentral Kocak N, Ozen F, Yildirim IH, Duran Y. Fentanyl inhibits tumorigenesis from human breast stem cells by inducing apoptosis. Asian Pac J Cancer Prev. 2017;18(3):735–9.PubMedPubMedCentral
56.
go back to reference Özgürbüz U, Gencür S, Kurt FÖ, Özkalkanlı M, Vatansever HS. The effects of tramadol on cancer stem cells and metabolic changes in colon carcinoma cells lines. Gene. 2019;718:144030.PubMed Özgürbüz U, Gencür S, Kurt FÖ, Özkalkanlı M, Vatansever HS. The effects of tramadol on cancer stem cells and metabolic changes in colon carcinoma cells lines. Gene. 2019;718:144030.PubMed
57.
go back to reference Xia L, Tan S, Zhou Y, Lin J, Wang H, Oyang L, et al. Role of the NFκB-signaling pathway in cancer. Onco Targets Ther. 2018;11:2063–73.PubMedPubMedCentral Xia L, Tan S, Zhou Y, Lin J, Wang H, Oyang L, et al. Role of the NFκB-signaling pathway in cancer. Onco Targets Ther. 2018;11:2063–73.PubMedPubMedCentral
58.
59.
go back to reference Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.PubMed Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.PubMed
60.
go back to reference Borner C, Kraus J. Inhibition of NF- B by opioids in T cells. J Immunol. 2013;191(9):4640–7.PubMed Borner C, Kraus J. Inhibition of NF- B by opioids in T cells. J Immunol. 2013;191(9):4640–7.PubMed
61.
go back to reference Qiu S, Feng Y, LeSage G, Zhang Y, Stuart C, He L, et al. Chronic morphine-induced microRNA-124 promotes microglial immunosuppression by modulating P65 and TRAF6. J Immunol. 2015;194(3):1021–30.PubMed Qiu S, Feng Y, LeSage G, Zhang Y, Stuart C, He L, et al. Chronic morphine-induced microRNA-124 promotes microglial immunosuppression by modulating P65 and TRAF6. J Immunol. 2015;194(3):1021–30.PubMed
62.
go back to reference Borner C, Hollt V, Kraus J. Mechanisms of the inhibition of nuclear factor- B by morphine in neuronal cells. Mol Pharmacol. 2012;81(4):587–97.PubMed Borner C, Hollt V, Kraus J. Mechanisms of the inhibition of nuclear factor- B by morphine in neuronal cells. Mol Pharmacol. 2012;81(4):587–97.PubMed
63.
go back to reference Welters ID, Menzebach A, Goumon Y, Cadet P, Menges T, Hughes TK, et al. Morphine inhibits NF-kappaB nuclear binding in human neutrophils and monocytes by a nitric oxide-dependent mechanism. Anesthesiology. 2000;92(6):1677–84.PubMed Welters ID, Menzebach A, Goumon Y, Cadet P, Menges T, Hughes TK, et al. Morphine inhibits NF-kappaB nuclear binding in human neutrophils and monocytes by a nitric oxide-dependent mechanism. Anesthesiology. 2000;92(6):1677–84.PubMed
64.
go back to reference Beltran JA, Peek J, Chang SL. Expression and regulation of the mu opioid peptide receptor in TPA-differentiated HL-60 promyelocytic leukemia cells. Int Immunopharmacol. 2006;6(8):1331–40.PubMed Beltran JA, Peek J, Chang SL. Expression and regulation of the mu opioid peptide receptor in TPA-differentiated HL-60 promyelocytic leukemia cells. Int Immunopharmacol. 2006;6(8):1331–40.PubMed
65.
go back to reference Ghosh N, Chaki R, Mandal V, Mandal SC. COX-2 as a target for cancer chemotherapy. Pharmacol Rep. 2010;62(2):233–44.PubMed Ghosh N, Chaki R, Mandal V, Mandal SC. COX-2 as a target for cancer chemotherapy. Pharmacol Rep. 2010;62(2):233–44.PubMed
66.
go back to reference Capasso A. The effect of morphine on the expression of COX-2 and iNOS enzymes. Cent Nerv Syst Agents Med Chem. 2008;8(1):1–9. Capasso A. The effect of morphine on the expression of COX-2 and iNOS enzymes. Cent Nerv Syst Agents Med Chem. 2008;8(1):1–9.
67.
go back to reference Waldman SA, Terzic A. A study of microRNAs in silico and in vivo: diagnostic and therapeutic applications in cancer. FEBS J. 2009;276(8):2157–64.PubMedPubMedCentral Waldman SA, Terzic A. A study of microRNAs in silico and in vivo: diagnostic and therapeutic applications in cancer. FEBS J. 2009;276(8):2157–64.PubMedPubMedCentral
68.
go back to reference Zhou T, Zhang G, Liu Z, Xia S, Tian H. Overexpression of miR-92a correlates with tumor metastasis and poor prognosis in patients with colorectal cancer. Int J Color Dis. 2013;28(1):19–24. Zhou T, Zhang G, Liu Z, Xia S, Tian H. Overexpression of miR-92a correlates with tumor metastasis and poor prognosis in patients with colorectal cancer. Int J Color Dis. 2013;28(1):19–24.
69.
go back to reference Kong W-Q, Bai R, Liu T, Cai C-L, Liu M, Li X, et al. MicroRNA-182 targets cAMP-responsive element-binding protein 1 and suppresses cell growth in human gastric adenocarcinoma. FEBS J. 2012;279(7):1252–60.PubMed Kong W-Q, Bai R, Liu T, Cai C-L, Liu M, Li X, et al. MicroRNA-182 targets cAMP-responsive element-binding protein 1 and suppresses cell growth in human gastric adenocarcinoma. FEBS J. 2012;279(7):1252–60.PubMed
70.
go back to reference Liu Z, Liu J, Segura MF, Shao C, Lee P, Gong Y, et al. MiR-182 overexpression in tumourigenesis of high-grade serous ovarian carcinoma. J Pathol. 2012;228(2):204–15.PubMed Liu Z, Liu J, Segura MF, Shao C, Lee P, Gong Y, et al. MiR-182 overexpression in tumourigenesis of high-grade serous ovarian carcinoma. J Pathol. 2012;228(2):204–15.PubMed
71.
go back to reference Pencheva N, Tavazoie SF. Control of metastatic progression by microRNA regulatory networks. Nat Cell Biol. 2013;15(6):546–54.PubMedPubMedCentral Pencheva N, Tavazoie SF. Control of metastatic progression by microRNA regulatory networks. Nat Cell Biol. 2013;15(6):546–54.PubMedPubMedCentral
72.
go back to reference Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med. 2009;60(1):167–79.PubMed Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med. 2009;60(1):167–79.PubMed
73.
go back to reference Zhang XL, Chen ML, Zhou SL. Fentanyl inhibits proliferation and invasion of colorectal cancer via β-catenin. Int J Clin Exp Pathol. 2015;8(1):227–35.PubMedPubMedCentral Zhang XL, Chen ML, Zhou SL. Fentanyl inhibits proliferation and invasion of colorectal cancer via β-catenin. Int J Clin Exp Pathol. 2015;8(1):227–35.PubMedPubMedCentral
74.
go back to reference Liu H, Du L, Wen Z, Yang Y, Li J, Wang L, et al. Up-regulation of miR-182 expression in colorectal cancer tissues and its prognostic value. Int J Color Dis. 2013;28(5):697–703. Liu H, Du L, Wen Z, Yang Y, Li J, Wang L, et al. Up-regulation of miR-182 expression in colorectal cancer tissues and its prognostic value. Int J Color Dis. 2013;28(5):697–703.
75.
go back to reference Wang N, Zhang Z, Lv J. Fentanyl inhibits proliferation and invasion via enhancing miR-302b expression in esophageal squamous cell carcinoma. Oncol Lett. 2018;16(1):459–66.PubMedPubMedCentral Wang N, Zhang Z, Lv J. Fentanyl inhibits proliferation and invasion via enhancing miR-302b expression in esophageal squamous cell carcinoma. Oncol Lett. 2018;16(1):459–66.PubMedPubMedCentral
76.
go back to reference Blebea J, Mazo JE, Kihara TK, Vu J-H, McLaughlin PJ, Atnip RG, et al. Opioid growth factor modulates angiogenesis. J Vasc Surg. 2000;32(2):364–73.PubMed Blebea J, Mazo JE, Kihara TK, Vu J-H, McLaughlin PJ, Atnip RG, et al. Opioid growth factor modulates angiogenesis. J Vasc Surg. 2000;32(2):364–73.PubMed
77.
go back to reference Dai X, Cui S, Wang T, Liu Q, Song H, Wang R. Endogenous opioid peptides, endomorphin-1 and -2 and deltorphin I, stimulate angiogenesis in the CAM assay. Eur J Pharmacol. 2008;579(1–3):269–75.PubMed Dai X, Cui S, Wang T, Liu Q, Song H, Wang R. Endogenous opioid peptides, endomorphin-1 and -2 and deltorphin I, stimulate angiogenesis in the CAM assay. Eur J Pharmacol. 2008;579(1–3):269–75.PubMed
78.
go back to reference • Yamamizu K, Hamada Y, Narita M. κ Opioid receptor ligands regulate angiogenesis in development and in tumours. Br J Pharmacol. 2015;172(2):268–76 In this study it was found that methadone may induce anti-inflammatory action during colonic inflammation through opioid receptors located mainly in the central nervous system.PubMed • Yamamizu K, Hamada Y, Narita M. κ Opioid receptor ligands regulate angiogenesis in development and in tumours. Br J Pharmacol. 2015;172(2):268–76 In this study it was found that methadone may induce anti-inflammatory action during colonic inflammation through opioid receptors located mainly in the central nervous system.PubMed
79.
go back to reference Ondrovics M, Hoelbl-Kovacic A, Fux DA. Opioids: modulators of angiogenesis in wound healing and cancer. Oncotarget. 2017;8(15):25783–96.PubMedPubMedCentral Ondrovics M, Hoelbl-Kovacic A, Fux DA. Opioids: modulators of angiogenesis in wound healing and cancer. Oncotarget. 2017;8(15):25783–96.PubMedPubMedCentral
80.
go back to reference Nguyen J, Luk K, Vang D, Soto W, Vincent L, Robiner S, et al. Morphine stimulates cancer progression and mast cell activation and impairs survival in transgenic mice with breast cancer. Br J Anaesth. 2014;113(Suppl 1):i4–13.PubMedPubMedCentral Nguyen J, Luk K, Vang D, Soto W, Vincent L, Robiner S, et al. Morphine stimulates cancer progression and mast cell activation and impairs survival in transgenic mice with breast cancer. Br J Anaesth. 2014;113(Suppl 1):i4–13.PubMedPubMedCentral
81.
go back to reference Koodie L, Ramakrishnan S, Roy S. Morphine suppresses tumor angiogenesis through a HIF-1alpha/p38MAPK pathway. Am J Pathol. 2010;177(2):984–97.PubMedPubMedCentral Koodie L, Ramakrishnan S, Roy S. Morphine suppresses tumor angiogenesis through a HIF-1alpha/p38MAPK pathway. Am J Pathol. 2010;177(2):984–97.PubMedPubMedCentral
82.
go back to reference Gupta K, Kshirsagar S, Chang L, Schwartz R, Law PY, Yee D, et al. Morphine stimulates angiogenesis by activating proangiogenic and survival-promoting signaling and promotes breast tumor growth. Cancer Res. 2002;62(15):4491–8.PubMed Gupta K, Kshirsagar S, Chang L, Schwartz R, Law PY, Yee D, et al. Morphine stimulates angiogenesis by activating proangiogenic and survival-promoting signaling and promotes breast tumor growth. Cancer Res. 2002;62(15):4491–8.PubMed
83.
go back to reference Martin JL, Charboneau R, Barke RA, Roy S. Chronic morphine treatment inhibits LPS-induced angiogenesis: implications in wound healing. Cell Immunol. 2010;265(2):139–45.PubMedPubMedCentral Martin JL, Charboneau R, Barke RA, Roy S. Chronic morphine treatment inhibits LPS-induced angiogenesis: implications in wound healing. Cell Immunol. 2010;265(2):139–45.PubMedPubMedCentral
84.
go back to reference Moradi M, Esmaeili S, Shoar S, Safari S. Use of oxycodone in pain management. Anesthesiol Pain Med. 2012;1(4):262–4. Moradi M, Esmaeili S, Shoar S, Safari S. Use of oxycodone in pain management. Anesthesiol Pain Med. 2012;1(4):262–4.
85.
go back to reference Geiger TR, Peeper DS. Metastasis mechanisms. Biochim Biophys Acta Rev Cancer. 2009:293–308. Geiger TR, Peeper DS. Metastasis mechanisms. Biochim Biophys Acta Rev Cancer. 2009:293–308.
86.
go back to reference Fagan-Solis KD, Schneider SS, Pentecost BT, Bentley BA, Otis CN, Gierthy JF, et al. The RhoA pathway mediates MMP-2 and MMP-9-independent invasive behavior in a triple-negative breast cancer cell line. J Cell Biochem. 2013;114(6):1385–94.PubMed Fagan-Solis KD, Schneider SS, Pentecost BT, Bentley BA, Otis CN, Gierthy JF, et al. The RhoA pathway mediates MMP-2 and MMP-9-independent invasive behavior in a triple-negative breast cancer cell line. J Cell Biochem. 2013;114(6):1385–94.PubMed
87.
go back to reference Engbring JA, Kleinman HK. The basement membrane matrix in malignancy. J Pathol. 2003:465–70.PubMed Engbring JA, Kleinman HK. The basement membrane matrix in malignancy. J Pathol. 2003:465–70.PubMed
88.
go back to reference Harimaya Y, Koizumi K, Andoh T, Nojima H, Kuraishi Y, Saiki I. Potential ability of morphine to inhibit the adhesion, invasion and metastasis of metastatic colon 26-L5 carcinoma cells. Cancer Lett. 2002;187(1–2):121–7.PubMed Harimaya Y, Koizumi K, Andoh T, Nojima H, Kuraishi Y, Saiki I. Potential ability of morphine to inhibit the adhesion, invasion and metastasis of metastatic colon 26-L5 carcinoma cells. Cancer Lett. 2002;187(1–2):121–7.PubMed
89.
go back to reference Nylund G, Pettersson A, Bengtsson C, Khorram-Manesh A, Nordgren S, Delbro DS. Functional expression of μ-opioid receptors in the human colon cancer cell line, HT-29, and their localization in human colon. Dig Dis Sci. 2008;53(2):461–6.PubMed Nylund G, Pettersson A, Bengtsson C, Khorram-Manesh A, Nordgren S, Delbro DS. Functional expression of μ-opioid receptors in the human colon cancer cell line, HT-29, and their localization in human colon. Dig Dis Sci. 2008;53(2):461–6.PubMed
90.
go back to reference • Khabbazi S, Hassanshahi M, Hassanshahi A, Peymanfar Y, Su Y-W, Xian CJ. Opioids and matrix metalloproteinases: the influence of morphine on MMP-9 production and cancer progression. Naunyn Schmiedeberg's Arch Pharmacol. 2019;392(2):123–33 In this review possible influence of opioids such as morphine on matrix metalloproteinases production through different molecular pathways has been discussed. • Khabbazi S, Hassanshahi M, Hassanshahi A, Peymanfar Y, Su Y-W, Xian CJ. Opioids and matrix metalloproteinases: the influence of morphine on MMP-9 production and cancer progression. Naunyn Schmiedeberg's Arch Pharmacol. 2019;392(2):123–33 In this review possible influence of opioids such as morphine on matrix metalloproteinases production through different molecular pathways has been discussed.
91.
go back to reference Tutton MG, George ML, Eccles SA, Burton S, Swift RI, Abulafi AM. Use of plasma MMP-2 and MMP-9 levels as a surrogate for tumour expression in colorectal cancer patients. Int J Cancer. 2003;107(4):541–50.PubMed Tutton MG, George ML, Eccles SA, Burton S, Swift RI, Abulafi AM. Use of plasma MMP-2 and MMP-9 levels as a surrogate for tumour expression in colorectal cancer patients. Int J Cancer. 2003;107(4):541–50.PubMed
92.
go back to reference Cata JP, Keerty V, Keerty D, Feng L, Norman PH, Gottumukkala V, et al. A retrospective analysis of the effect of intraoperative opioid dose on cancer recurrence after non-small cell lung cancer resection. Cancer Med. 2014;3(4):900–8.PubMedPubMedCentral Cata JP, Keerty V, Keerty D, Feng L, Norman PH, Gottumukkala V, et al. A retrospective analysis of the effect of intraoperative opioid dose on cancer recurrence after non-small cell lung cancer resection. Cancer Med. 2014;3(4):900–8.PubMedPubMedCentral
93.
go back to reference Hasegawa T, Oguri T, Osawa T, Sawa T, Osaga S, Okuyama T, et al. Opioid dose and survival of patients with incurable nonsmall cell lung cancer: a prospective cohort study. J Palliat Med. 2018;21(10):1436–41.PubMed Hasegawa T, Oguri T, Osawa T, Sawa T, Osaga S, Okuyama T, et al. Opioid dose and survival of patients with incurable nonsmall cell lung cancer: a prospective cohort study. J Palliat Med. 2018;21(10):1436–41.PubMed
94.
go back to reference Janku F, Johnson LK, Karp DD, Atkins JT, Singleton PA, Moss J. Treatment with methylnaltrexone is associated with increased survival in patients with advanced cancer. Ann Oncol Off J Eur Soc Med Oncol. 2016;27(11):2032–8. Janku F, Johnson LK, Karp DD, Atkins JT, Singleton PA, Moss J. Treatment with methylnaltrexone is associated with increased survival in patients with advanced cancer. Ann Oncol Off J Eur Soc Med Oncol. 2016;27(11):2032–8.
95.
go back to reference Sathornviriyapong A, Nagaviroj K, Anothaisintawee T. The association between different opioid doses and the survival of advanced cancer patients receiving palliative care. BMC Palliat Care. 2016;15(1):95.PubMedPubMedCentral Sathornviriyapong A, Nagaviroj K, Anothaisintawee T. The association between different opioid doses and the survival of advanced cancer patients receiving palliative care. BMC Palliat Care. 2016;15(1):95.PubMedPubMedCentral
96.
go back to reference Sessler DI, Pei L, Huang Y, Fleischmann E, Marhofer P, Kurz A, et al. Recurrence of breast cancer after regional or general anaesthesia: a randomised controlled trial. Lancet. 2019;394(10211):1807–15.PubMed Sessler DI, Pei L, Huang Y, Fleischmann E, Marhofer P, Kurz A, et al. Recurrence of breast cancer after regional or general anaesthesia: a randomised controlled trial. Lancet. 2019;394(10211):1807–15.PubMed
97.
go back to reference Sekandarzad MW, Doornebal C, Hollmann MW. Opiophobia in cancer biology- justified? - the role of perioperative use of opioids in cancer recurrence. Curr Pharm Des. 2019;25(28):3020–7.PubMed Sekandarzad MW, Doornebal C, Hollmann MW. Opiophobia in cancer biology- justified? - the role of perioperative use of opioids in cancer recurrence. Curr Pharm Des. 2019;25(28):3020–7.PubMed
98.
go back to reference Cao L-H, Li H-T, Lin W-Q, Tan H-Y, Xie L, Zhong Z-J, et al. Morphine, a potential antagonist of cisplatin cytotoxicity, inhibits cisplatin-induced apoptosis and suppression of tumor growth in nasopharyngeal carcinoma xenografts. Sci Rep. 2016;6:18706.PubMedPubMedCentral Cao L-H, Li H-T, Lin W-Q, Tan H-Y, Xie L, Zhong Z-J, et al. Morphine, a potential antagonist of cisplatin cytotoxicity, inhibits cisplatin-induced apoptosis and suppression of tumor growth in nasopharyngeal carcinoma xenografts. Sci Rep. 2016;6:18706.PubMedPubMedCentral
99.
go back to reference He B, Tong X, Wang L, Wang Q, Ye H, Liu B, et al. Tramadol and flurbiprofen depress the cytotoxicity of cisplatin via their effects on gap junctions. Clin Cancer Res. 2009;15(18):5803–10.PubMed He B, Tong X, Wang L, Wang Q, Ye H, Liu B, et al. Tramadol and flurbiprofen depress the cytotoxicity of cisplatin via their effects on gap junctions. Clin Cancer Res. 2009;15(18):5803–10.PubMed
Metadata
Title
Opioids in Cancer Development, Progression and Metastasis: Focus on Colorectal Cancer
Authors
Adrian Szczepaniak
Jakub Fichna, PhD, DSc
Marta Zielińska, PhD
Publication date
01-01-2020
Publisher
Springer US
Published in
Current Treatment Options in Oncology / Issue 1/2020
Print ISSN: 1527-2729
Electronic ISSN: 1534-6277
DOI
https://doi.org/10.1007/s11864-019-0699-1

Other articles of this Issue 1/2020

Current Treatment Options in Oncology 1/2020 Go to the issue

Leukemia (PH Wiernik, Section Editor)

The Microbiota in Hematologic Malignancies

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine