Skip to main content
Top
Published in: Clinical and Translational Oncology 6/2019

Open Access 01-06-2019 | Review Article

The dual effect of morphine on tumor development

Authors: H. Tuerxun, J. Cui

Published in: Clinical and Translational Oncology | Issue 6/2019

Login to get access

Abstract

Morphine is a classic opioid drug used for reducing pain and is commonly prescribed as an effective drug to control cancer pain. Morphine has a direct role in the central nervous system to relieve pain, but because of its peripheral functions, morphine also has some side effects, such as nausea, constipation, and addiction (Gupta et al. in Sci World J 2015:10, 2015). In addition to its analgesic effect, the role of morphine in tumor development is an important question that has been investigated for many years with conflicting results. Numerous studies suggest that morphine has a role in both promoting and inhibiting tumor growth. In this extensive review, we attempt to comprehensively understand the effects of morphine and summarize both its positive and negative influences on various aspects of tumors, including tumor growth, angiogenesis, metastasis, inflammation, and immunomodulation.
Literature
1.
go back to reference Gupta M, Msambichaka L, Ballas SK, Gupta K. Morphine for the treatment of pain in sickle cell disease. Sci World J. 2015;2015:10.CrossRef Gupta M, Msambichaka L, Ballas SK, Gupta K. Morphine for the treatment of pain in sickle cell disease. Sci World J. 2015;2015:10.CrossRef
2.
go back to reference Shen LD, Yang J, Li YX, et al. Correlation between senile cancer pain and depression and its effect on immune function[J]. J Kunming Med Coll. 2011;2(3):31–4. Shen LD, Yang J, Li YX, et al. Correlation between senile cancer pain and depression and its effect on immune function[J]. J Kunming Med Coll. 2011;2(3):31–4.
3.
go back to reference Grace Peter M, Maier Steven F, Watkins Linda R. Opioid-induced central immune signaling: implications for opioid analgesia. Headache. 2015;55(4):475–89.CrossRef Grace Peter M, Maier Steven F, Watkins Linda R. Opioid-induced central immune signaling: implications for opioid analgesia. Headache. 2015;55(4):475–89.CrossRef
4.
go back to reference Tegeder I, Grosch S, Schmidtko A, Haussler A, Schmidt H, Niederberger E, Scholich K, Geisslinger G. G protein-independent G1 cell cycle block and apoptosis with morphine in adenocarcinoma cell:involvement of p53 phosphorylation. Cancer Res. 2003;63(8):1846–52.PubMed Tegeder I, Grosch S, Schmidtko A, Haussler A, Schmidt H, Niederberger E, Scholich K, Geisslinger G. G protein-independent G1 cell cycle block and apoptosis with morphine in adenocarcinoma cell:involvement of p53 phosphorylation. Cancer Res. 2003;63(8):1846–52.PubMed
5.
go back to reference Gonzalez-Nunez Veronica, Noriega-Prieto Jose Antonio, Rodríguez Raquel E. Morphine modulates cell proliferation through mir133b & mir128 in the neuroblastoma SH-SY5Y cell line. Biochim Biophys Acta Mol Basis Dis. 2014;1842(4):566–72.CrossRef Gonzalez-Nunez Veronica, Noriega-Prieto Jose Antonio, Rodríguez Raquel E. Morphine modulates cell proliferation through mir133b & mir128 in the neuroblastoma SH-SY5Y cell line. Biochim Biophys Acta Mol Basis Dis. 2014;1842(4):566–72.CrossRef
6.
go back to reference Hatzoglou A, Bakogeorgou E, Castanas E. The antiproliferative effect of opioid receptor agonists on the T47D human breast cancer cell line, is partially mediated through opioid receptors. Eur J Pharmacol. 1996;296(2):199–207.CrossRef Hatzoglou A, Bakogeorgou E, Castanas E. The antiproliferative effect of opioid receptor agonists on the T47D human breast cancer cell line, is partially mediated through opioid receptors. Eur J Pharmacol. 1996;296(2):199–207.CrossRef
7.
go back to reference Lin X, Wang YJ, Li Q, Hou YY, Hong MH, Cao YL, Chi ZQ, Liu JG. Chronic high-dose morphine treatment promotes SH-SY5Y cell apoptosis via c-Jun N-terminal kinase-mediated activation of mitochondria-dependent pathway. FEBS J. 2009;276(7):2022–36.CrossRef Lin X, Wang YJ, Li Q, Hou YY, Hong MH, Cao YL, Chi ZQ, Liu JG. Chronic high-dose morphine treatment promotes SH-SY5Y cell apoptosis via c-Jun N-terminal kinase-mediated activation of mitochondria-dependent pathway. FEBS J. 2009;276(7):2022–36.CrossRef
8.
go back to reference Yin D, Mufson RA, Wang R, Shi Y. Fas-mediated cell death promoted by opioids. Nature. 1999;397(6716):218.CrossRef Yin D, Mufson RA, Wang R, Shi Y. Fas-mediated cell death promoted by opioids. Nature. 1999;397(6716):218.CrossRef
9.
go back to reference Pati ML, Hornick JR, Niso M, Berardi F, Spitzer D. Sigma-2 receptor agonist derivatives of 1-Cyclohexyl-4-[3-(5-methoxy-1,2,3,4-tetrahydronaphthalen-1-yl)propyl]piperazine (PB28) induce cell death via mitochondrial superoxide production and caspase activation in pancreatic cancer. BMC Cancer. 2017;17(1):51.CrossRef Pati ML, Hornick JR, Niso M, Berardi F, Spitzer D. Sigma-2 receptor agonist derivatives of 1-Cyclohexyl-4-[3-(5-methoxy-1,2,3,4-tetrahydronaphthalen-1-yl)propyl]piperazine (PB28) induce cell death via mitochondrial superoxide production and caspase activation in pancreatic cancer. BMC Cancer. 2017;17(1):51.CrossRef
10.
go back to reference Diao CT, Li L, Lau SY, Wong TM, Wong NS. kappa-Opioid receptor potentiates apoptosis via a phospholipase C pathway in the CNE2 humanepithelial tumor cell line. Biochim Biophys Acta. 2000;1499(1–2):49–62.CrossRef Diao CT, Li L, Lau SY, Wong TM, Wong NS. kappa-Opioid receptor potentiates apoptosis via a phospholipase C pathway in the CNE2 humanepithelial tumor cell line. Biochim Biophys Acta. 2000;1499(1–2):49–62.CrossRef
11.
go back to reference Hatsukari Ikusuke, Hitosugi Naoko, Ohno Rie, Hashimoto Ken, Nakamura Shinichi, Satoh Kazue, Nagasaka Hiroshi, Matsumoto Isao, Sakagami Hiroshi. Induction of apoptosis by morphine in human tumor cell lines in vitro. Anticancer Res. 2007;27(2):857–64.PubMed Hatsukari Ikusuke, Hitosugi Naoko, Ohno Rie, Hashimoto Ken, Nakamura Shinichi, Satoh Kazue, Nagasaka Hiroshi, Matsumoto Isao, Sakagami Hiroshi. Induction of apoptosis by morphine in human tumor cell lines in vitro. Anticancer Res. 2007;27(2):857–64.PubMed
12.
go back to reference Sergeeva MG, Grishina ZV, Varfolomeyev SD. Morphine effect on proliferation of normal and tumor cells of immune origin. Immunol Lett. 1993;36(2):215–8.CrossRef Sergeeva MG, Grishina ZV, Varfolomeyev SD. Morphine effect on proliferation of normal and tumor cells of immune origin. Immunol Lett. 1993;36(2):215–8.CrossRef
13.
go back to reference Bimonte Sabrina, Barbieri Antonio, Rea Domenica, Palma Giuseppe, Luciano Antonio, Cuomo Arturo, Arra Claudio, Izzo Francesco. Morphine Promotes Tumor Angiogenesis and Increases Breast Cancer Progression. Biomed Res Int. 2015;2015:161508.PubMedPubMedCentral Bimonte Sabrina, Barbieri Antonio, Rea Domenica, Palma Giuseppe, Luciano Antonio, Cuomo Arturo, Arra Claudio, Izzo Francesco. Morphine Promotes Tumor Angiogenesis and Increases Breast Cancer Progression. Biomed Res Int. 2015;2015:161508.PubMedPubMedCentral
14.
go back to reference Cao LH, Li HT, Lin WQ, 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.CrossRef Cao LH, Li HT, Lin WQ, 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.CrossRef
15.
go back to reference Mathew B, Lennon FE, Siegler J, Mambetsariev N, et al. The novel role of the mu opioid receptor in lung cancer progression: a laboratory investigation. Anesth Analg. 2011;112(3):558–67.CrossRef Mathew B, Lennon FE, Siegler J, Mambetsariev N, et al. The novel role of the mu opioid receptor in lung cancer progression: a laboratory investigation. Anesth Analg. 2011;112(3):558–67.CrossRef
16.
go back to reference Fujioka N, Nguyen J, Chen C, Li Y, Pasrija T, Niehans G, Johnson K, Gupta V, Kratzke R, Kalpna G. Morphine-induced epidermal growth factor pathway activation in non-small cell lung cell. Anesth Analg. 2011;113(6):1353–64.CrossRef Fujioka N, Nguyen J, Chen C, Li Y, Pasrija T, Niehans G, Johnson K, Gupta V, Kratzke R, Kalpna G. Morphine-induced epidermal growth factor pathway activation in non-small cell lung cell. Anesth Analg. 2011;113(6):1353–64.CrossRef
17.
go back to reference Vincent L, Vang D, Nguyen J, et al. Mast cell activation contributes to sickle cell pathobiology and pain in mice. Blood. 2013;122:1853–62.CrossRef Vincent L, Vang D, Nguyen J, et al. Mast cell activation contributes to sickle cell pathobiology and pain in mice. Blood. 2013;122:1853–62.CrossRef
18.
go back to reference Aich A, Afrin LB, Gupta K. Mast cell-mediated mechanisms of nociception. Int J Mol Sci. 2015;16:29069–92.CrossRef Aich A, Afrin LB, Gupta K. Mast cell-mediated mechanisms of nociception. Int J Mol Sci. 2015;16:29069–92.CrossRef
19.
go back to reference Muñoz M, Coveñas R. Involvement of substance P and the NK-1 receptor in cancer progression. Peptides. 2013;48:1–9.CrossRef Muñoz M, Coveñas R. Involvement of substance P and the NK-1 receptor in cancer progression. Peptides. 2013;48:1–9.CrossRef
20.
go back to reference Lin X, Li Q, Wang YJ, Ju YW, Chi ZQ, Wang MW, Liu JG. Morphine inhibits doxorubicin-induced reactive oxygen species generation and nuclear factor kappaB transcriptional activation in neuroblastoma SH-SY5Y cells. Biochem J. 2007;406(2):215–21.CrossRef Lin X, Li Q, Wang YJ, Ju YW, Chi ZQ, Wang MW, Liu JG. Morphine inhibits doxorubicin-induced reactive oxygen species generation and nuclear factor kappaB transcriptional activation in neuroblastoma SH-SY5Y cells. Biochem J. 2007;406(2):215–21.CrossRef
21.
go back to reference Ma Y, Ren Z, Ma S, Yan W, He M, Wang D, Ding P. Morphine enhances renal cell carcinoma aggressiveness through promotes survivin level. Ren Fail. 2017;39(1):258–64.CrossRef Ma Y, Ren Z, Ma S, Yan W, He M, Wang D, Ding P. Morphine enhances renal cell carcinoma aggressiveness through promotes survivin level. Ren Fail. 2017;39(1):258–64.CrossRef
22.
go back to reference Folkman J, D’Amore PA. Blood vessel formation: what is its molecular basis? Cell. 1996;87(7):1153–5.CrossRef Folkman J, D’Amore PA. Blood vessel formation: what is its molecular basis? Cell. 1996;87(7):1153–5.CrossRef
23.
go back to reference Brekken RA, Thorpe PE. Vascular endothelial growth factor and vascular targeting of solid tumors. Anticancer Res. 2001;21(6b):4221–9.PubMed Brekken RA, Thorpe PE. Vascular endothelial growth factor and vascular targeting of solid tumors. Anticancer Res. 2001;21(6b):4221–9.PubMed
24.
go back to reference Balasubramanian S, Ramakrishnan S, Charboneau R, Wang J, Barke RA, Roy S. Morphine sulfate inhibits hypoxia-induced vascular endothelial growth factor expression in endothelial cells and cardiac myocytes. J Mol Cell Cardiol. 2001;33:2179–87.CrossRef Balasubramanian S, Ramakrishnan S, Charboneau R, Wang J, Barke RA, Roy S. Morphine sulfate inhibits hypoxia-induced vascular endothelial growth factor expression in endothelial cells and cardiac myocytes. J Mol Cell Cardiol. 2001;33:2179–87.CrossRef
25.
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.CrossRef Koodie L, Ramakrishnan S, Roy S. Morphine suppresses tumor angiogenesis through a HIF-1alpha/p38MAPK pathway. Am J Pathol. 2010;177(2):984–97.CrossRef
26.
go back to reference Yamamizu K, Hamada Y, Narita M. j Opioid receptor ligands regulate angiogenesis in development and in tumours. Br J Pharmacol. 2015;172(2):268–76.CrossRef Yamamizu K, Hamada Y, Narita M. j Opioid receptor ligands regulate angiogenesis in development and in tumours. Br J Pharmacol. 2015;172(2):268–76.CrossRef
27.
go back to reference Koodie L, Yuan H, Pumper JA, et al. Morphine inhibits migration of tumor-infiltrating leukocytes and suppresses angiogenesis associated with tumor growth in mice. Am J Pathol. 2014;184:1073–84.CrossRef Koodie L, Yuan H, Pumper JA, et al. Morphine inhibits migration of tumor-infiltrating leukocytes and suppresses angiogenesis associated with tumor growth in mice. Am J Pathol. 2014;184:1073–84.CrossRef
28.
go back to reference Singleton PA, Moss J. Effect of perioperative opioids on cancer recurrence: a hypothesis. Future Oncol. 2010;6(8):1237–42.CrossRef Singleton PA, Moss J. Effect of perioperative opioids on cancer recurrence: a hypothesis. Future Oncol. 2010;6(8):1237–42.CrossRef
29.
go back to reference Kevil CG, Orr AW, Langston W, Mickett K, Murphy-Ullrich J, Patel RP, et al. Intercellular adhesion molecule-1 (ICAM-1) regulates endothelial cell motility through a nitric oxide-dependent pathway. J Biol Chem. 2004;279(18):19230–8.CrossRef Kevil CG, Orr AW, Langston W, Mickett K, Murphy-Ullrich J, Patel RP, et al. Intercellular adhesion molecule-1 (ICAM-1) regulates endothelial cell motility through a nitric oxide-dependent pathway. J Biol Chem. 2004;279(18):19230–8.CrossRef
30.
31.
go back to reference Farooqui M, Li Y, Rogers T, Poonawala T, Griffin RJ, Song CW, et al. COX-2 inhibitor celecoxib prevents chronic morphine-induced promotion of angiogenesis, tumour growth, metastasis and mortality, without compromising analgesia. Br J Cancer. 2007;97(11):1523–31.CrossRef Farooqui M, Li Y, Rogers T, Poonawala T, Griffin RJ, Song CW, et al. COX-2 inhibitor celecoxib prevents chronic morphine-induced promotion of angiogenesis, tumour growth, metastasis and mortality, without compromising analgesia. Br J Cancer. 2007;97(11):1523–31.CrossRef
32.
go back to reference Yamamoto Kazuhiro, Murphy Gillian, Troeberg Linda. Extracellular regulation of metalloproteinases. Matrix Biol. 2015;44–46:255–63.CrossRef Yamamoto Kazuhiro, Murphy Gillian, Troeberg Linda. Extracellular regulation of metalloproteinases. Matrix Biol. 2015;44–46:255–63.CrossRef
33.
go back to reference Gouri Adel, Dekaken Aoulia, El Bairi Khalid, Aissaoui Arifa, Laabed Nihad, Chefrour Mohamed, Ciccolini Joseph, Milano Gérard, Benharkat Sadek. Plasminogen activator system and breast cancer: potential role in therapy decision making and precision medicine. Biomarker Insight. 2016;11:105–11.CrossRef Gouri Adel, Dekaken Aoulia, El Bairi Khalid, Aissaoui Arifa, Laabed Nihad, Chefrour Mohamed, Ciccolini Joseph, Milano Gérard, Benharkat Sadek. Plasminogen activator system and breast cancer: potential role in therapy decision making and precision medicine. Biomarker Insight. 2016;11:105–11.CrossRef
34.
go back to reference Xie Nan, Khabbazi Samira, Nassar Zeyad D, Gregory Kye, Vithanage Tharindu, Anand-Apte Bela, Cabot Peter J, Sturgess David, Shaw Paul N, Parat Marie-Odile. Morphine alters the circulating proteolytic profile in mice: functional consequences on cellular migration and invasion. FASEB J. 2017;31(12):5208–16.CrossRef Xie Nan, Khabbazi Samira, Nassar Zeyad D, Gregory Kye, Vithanage Tharindu, Anand-Apte Bela, Cabot Peter J, Sturgess David, Shaw Paul N, Parat Marie-Odile. Morphine alters the circulating proteolytic profile in mice: functional consequences on cellular migration and invasion. FASEB J. 2017;31(12):5208–16.CrossRef
35.
go back to reference Gach Katarzyna, Szemraj Janusz, Wyrębska Anna, Janecka Anna. The influence of opioids on matrix metalloproteinase-2 and -9 secretion and mRNA levels in MCF-7 breast cancer cell line. Mol Biol Rep. 2011;38(2):1231–6.CrossRef Gach Katarzyna, Szemraj Janusz, Wyrębska Anna, Janecka Anna. The influence of opioids on matrix metalloproteinase-2 and -9 secretion and mRNA levels in MCF-7 breast cancer cell line. Mol Biol Rep. 2011;38(2):1231–6.CrossRef
36.
go back to reference Min Too Jae, Park Sang-Hee, Ji Yi-Hwa, Lee Yoon-Sook, Kim Tae Woo, Kim Jae Hwan, Kim Woon-Young, Park Young-Cheol. Morphine attenuates endothelial cell adhesion molecules induced by the supernatant of LPS-stimulated colon cancer cells. J Korean Med Sci. 2011;26(6):747–52.CrossRef Min Too Jae, Park Sang-Hee, Ji Yi-Hwa, Lee Yoon-Sook, Kim Tae Woo, Kim Jae Hwan, Kim Woon-Young, Park Young-Cheol. Morphine attenuates endothelial cell adhesion molecules induced by the supernatant of LPS-stimulated colon cancer cells. J Korean Med Sci. 2011;26(6):747–52.CrossRef
37.
go back to reference Gach K, Szemraj J, Fichna J, Piestrzeniewicz M, Delbro DS, Janecka A. The influence of opioids on urokinase plasminogen activator on protein and mRNA level in MCF-7 breast cancer cell line. Chem Biol Drug Des. 2009;74(4):390–6.CrossRef Gach K, Szemraj J, Fichna J, Piestrzeniewicz M, Delbro DS, Janecka A. The influence of opioids on urokinase plasminogen activator on protein and mRNA level in MCF-7 breast cancer cell line. Chem Biol Drug Des. 2009;74(4):390–6.CrossRef
38.
go back to reference Nylund G, Pettersson A, Bengtsson C, Khorram-Manesh A, Nordgren S, Delbro DS. Functional expression of mu-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.CrossRef Nylund G, Pettersson A, Bengtsson C, Khorram-Manesh A, Nordgren S, Delbro DS. Functional expression of mu-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.CrossRef
39.
go back to reference Liu S, Qi L, Yu Q, et al. Survivin and HLA-I expression predicts survival of patients with clear cell renal cell carcinoma. Tumour Biol. 2014;35:8281–8.CrossRef Liu S, Qi L, Yu Q, et al. Survivin and HLA-I expression predicts survival of patients with clear cell renal cell carcinoma. Tumour Biol. 2014;35:8281–8.CrossRef
40.
go back to reference Chen X, Chen XG, Hu X, et al. MiR-34a and miR-203 inhibit survivin expression to control cell proliferation and survival in human osteosarcoma cells. J Cancer. 2016;7:1057–65.CrossRef Chen X, Chen XG, Hu X, et al. MiR-34a and miR-203 inhibit survivin expression to control cell proliferation and survival in human osteosarcoma cells. J Cancer. 2016;7:1057–65.CrossRef
41.
go back to reference Boettger MK, Weber K, Gajda M, Brauer R, Schaible HG. Spinally applied ketamine or morphine attenuate peripheral inflammation and hyperalgesia in acute and chronic phases of experimental arthritis. Brain Behav Immun. 2010;24(3):474–85.CrossRef Boettger MK, Weber K, Gajda M, Brauer R, Schaible HG. Spinally applied ketamine or morphine attenuate peripheral inflammation and hyperalgesia in acute and chronic phases of experimental arthritis. Brain Behav Immun. 2010;24(3):474–85.CrossRef
42.
go back to reference Cabot PJ, Carter L, Gaiddon C, Zhang Q, Schafer M, Loeffler JP, Stein C. Immune cell-derived beta-endorphin. Production, release, and control of inflammatory pain in rats. J Clin Invest. 1997;100(1):142–8.CrossRef Cabot PJ, Carter L, Gaiddon C, Zhang Q, Schafer M, Loeffler JP, Stein C. Immune cell-derived beta-endorphin. Production, release, and control of inflammatory pain in rats. J Clin Invest. 1997;100(1):142–8.CrossRef
43.
go back to reference Finley MJ, Happel CM, Kaminsky DE, Rogers TJ. Opioid and nociceptin receptors regulate cytokine and cytokine receptor expression. Cell Immunol. 2008;252(1–2):146–54.CrossRef Finley MJ, Happel CM, Kaminsky DE, Rogers TJ. Opioid and nociceptin receptors regulate cytokine and cytokine receptor expression. Cell Immunol. 2008;252(1–2):146–54.CrossRef
44.
go back to reference Sabita R, Jinghua W, Jennifer K, Lisa K, Josephine M. Modulation of immune function by morphine: implications for susceptibility to infection. J Neuroimmun Pharmacol. 2006;1:77–89.CrossRef Sabita R, Jinghua W, Jennifer K, Lisa K, Josephine M. Modulation of immune function by morphine: implications for susceptibility to infection. J Neuroimmun Pharmacol. 2006;1:77–89.CrossRef
45.
go back to reference Roy S, Wang J, Kelschenbach J, Koodie L, Martin J. Modulation of immune function by morphine: implications for susceptibility to infection. J Neuroimmune Pharmacol. 2006;1:77–89.CrossRef Roy S, Wang J, Kelschenbach J, Koodie L, Martin J. Modulation of immune function by morphine: implications for susceptibility to infection. J Neuroimmune Pharmacol. 2006;1:77–89.CrossRef
46.
go back to reference Grimm MC, Ben-Baruch A, Taub DD, Howard OM, Resau JH, Wang JM, Ali H, Richardson R, Snyderman R, Oppenheim JJ. Opiates transdeactivate chemokine receptors: delta and mu opiate receptor-mediated heterologous desensitization. J Exp Med. 1998;188:317–25.CrossRef Grimm MC, Ben-Baruch A, Taub DD, Howard OM, Resau JH, Wang JM, Ali H, Richardson R, Snyderman R, Oppenheim JJ. Opiates transdeactivate chemokine receptors: delta and mu opiate receptor-mediated heterologous desensitization. J Exp Med. 1998;188:317–25.CrossRef
47.
go back to reference Ninkovic J, Roy S. Role of the mu-opioid receptor in opioid modulation of immune function. Amino Acids. 2013;45:9–24.CrossRef Ninkovic J, Roy S. Role of the mu-opioid receptor in opioid modulation of immune function. Amino Acids. 2013;45:9–24.CrossRef
48.
go back to reference Menzebach A, Hirsch J, Nost R, Mogk M, Hempelmann G, Welters ID. Morphine inhibits complement receptor expression, phagocytosis and oxidative burst by a nitric oxide dependent mechanism. Anasthesiol Intensivmed Notfallmed Schmerzther. 2004;39:204–11.CrossRef Menzebach A, Hirsch J, Nost R, Mogk M, Hempelmann G, Welters ID. Morphine inhibits complement receptor expression, phagocytosis and oxidative burst by a nitric oxide dependent mechanism. Anasthesiol Intensivmed Notfallmed Schmerzther. 2004;39:204–11.CrossRef
49.
go back to reference Tabellini G, Borsani E, Benassi M, et al. Effects of opioid therapy on human natural killer cells. Int Immunopharmacol. 2014;18:169–74.CrossRef Tabellini G, Borsani E, Benassi M, et al. Effects of opioid therapy on human natural killer cells. Int Immunopharmacol. 2014;18:169–74.CrossRef
50.
go back to reference Ninković Jana, Roy Sabita. Role of the mu-opioid receptor in opioid modulation of immune function. Amino Acids. 2013;45(1):9–24.CrossRef Ninković Jana, Roy Sabita. Role of the mu-opioid receptor in opioid modulation of immune function. Amino Acids. 2013;45(1):9–24.CrossRef
51.
go back to reference Machelska H, Cabot PJ, Mousa SA, Zhang Q, Stein C. Pain control in inflammation governed by selectins. Nat Med. 1998;4:1425–8.CrossRef Machelska H, Cabot PJ, Mousa SA, Zhang Q, Stein C. Pain control in inflammation governed by selectins. Nat Med. 1998;4:1425–8.CrossRef
52.
go back to reference Roy S, Chapin RB, Cain KJ, Charboneau RG, Ramakrishnan S, Barke RA. Morphine inhibits transcriptional activation of IL-2 in mouse thymocytes. Cell Immunol. 1997;179:1–9.CrossRef Roy S, Chapin RB, Cain KJ, Charboneau RG, Ramakrishnan S, Barke RA. Morphine inhibits transcriptional activation of IL-2 in mouse thymocytes. Cell Immunol. 1997;179:1–9.CrossRef
53.
go back to reference Liang Xuan, Liu Renyu, Chen Chunhua, Ji Fang, Li Tianzuo. Opioid system modulates the immune function: a review. Trans Perioperat Pain Med. 2016;1(1):5–13. Liang Xuan, Liu Renyu, Chen Chunhua, Ji Fang, Li Tianzuo. Opioid system modulates the immune function: a review. Trans Perioperat Pain Med. 2016;1(1):5–13.
54.
go back to reference Weber RJ, Pert A. The periaqueductal gray matter mediates opiate-induced immunosuppression. Science. 1989;245:188–90.CrossRef Weber RJ, Pert A. The periaqueductal gray matter mediates opiate-induced immunosuppression. Science. 1989;245:188–90.CrossRef
55.
go back to reference Irwin M, Hauger RL, Brown M, Britton KT. CRF activates autonomic nervous system and reduces natural killer cytotoxicity. Am J Physiol. 1988;255(5 Pt 2):R744–7.PubMed Irwin M, Hauger RL, Brown M, Britton KT. CRF activates autonomic nervous system and reduces natural killer cytotoxicity. Am J Physiol. 1988;255(5 Pt 2):R744–7.PubMed
56.
go back to reference Hernandez MC, Flores LR, Bayer BM. Immunosuppression by morphine is mediated by central pathways. J Pharmacol Exp Ther. 1993;267:1336–41.PubMed Hernandez MC, Flores LR, Bayer BM. Immunosuppression by morphine is mediated by central pathways. J Pharmacol Exp Ther. 1993;267:1336–41.PubMed
57.
go back to reference Saurer TB, Ijames SG, Lysle DT. Neuropeptide Y Y1 receptors mediate morphine-induced reductions of natural killer cell activity. J Neuroimmunol. 2006;177:18–26.CrossRef Saurer TB, Ijames SG, Lysle DT. Neuropeptide Y Y1 receptors mediate morphine-induced reductions of natural killer cell activity. J Neuroimmunol. 2006;177:18–26.CrossRef
58.
go back to reference Fecho K, Maslonek KA, Dykstra LA, Lysle DT. Evidence for sympathetic and adrenal involvement in the immunomodulatory effects of acute morphine treatment in rats. J Pharmacol Exp Ther. 1996;277:633–45.PubMed Fecho K, Maslonek KA, Dykstra LA, Lysle DT. Evidence for sympathetic and adrenal involvement in the immunomodulatory effects of acute morphine treatment in rats. J Pharmacol Exp Ther. 1996;277:633–45.PubMed
59.
go back to reference Mellon RD, Bayer BM. Role of central opioid receptor subtypes in morphine-induced alterations in peripheral lymphocyte activity. Brain Res. 1998;789:56–67.CrossRef Mellon RD, Bayer BM. Role of central opioid receptor subtypes in morphine-induced alterations in peripheral lymphocyte activity. Brain Res. 1998;789:56–67.CrossRef
60.
go back to reference Zylla D, Gourley BL, Vang D, et al. Opioid requirement, opioid receptor expression, and clinical outcomes in patients with advanced prostate cancer. Cancer. 2013;119:4103–10.CrossRef Zylla D, Gourley BL, Vang D, et al. Opioid requirement, opioid receptor expression, and clinical outcomes in patients with advanced prostate cancer. Cancer. 2013;119:4103–10.CrossRef
61.
go back to reference Zylla D, Ma Kuskowski, Gupta K, Gupta P. Association of opioid requirement and cancer pain with survival in advanced non-small cell lung cancer. Br J Anaesth. 2014;113:1–8.CrossRef Zylla D, Ma Kuskowski, Gupta K, Gupta P. Association of opioid requirement and cancer pain with survival in advanced non-small cell lung cancer. Br J Anaesth. 2014;113:1–8.CrossRef
Metadata
Title
The dual effect of morphine on tumor development
Authors
H. Tuerxun
J. Cui
Publication date
01-06-2019
Publisher
Springer International Publishing
Published in
Clinical and Translational Oncology / Issue 6/2019
Print ISSN: 1699-048X
Electronic ISSN: 1699-3055
DOI
https://doi.org/10.1007/s12094-018-1974-5

Other articles of this Issue 6/2019

Clinical and Translational Oncology 6/2019 Go to the issue
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