Advertisement

Hormones and Cancer

, Volume 8, Issue 3, pp 143–156 | Cite as

Growth Hormone Receptor Knockdown Sensitizes Human Melanoma Cells to Chemotherapy by Attenuating Expression of ABC Drug Efflux Pumps

  • Reetobrata Basu
  • Nicholas Baumgaertel
  • Shiyong Wu
  • John J. KopchickEmail author
Original Paper

Abstract

Melanoma remains one of the most therapy-resistant forms of human cancer despite recent introductions of highly efficacious targeted therapies. The intrinsic therapy resistance of human melanoma is largely due to abundant expression of a repertoire of xenobiotic efflux pumps of the ATP-binding cassette (ABC) transporter family. Here, we report that GH action is a key mediator of chemotherapeutic resistance in human melanoma cells. We investigated multiple ABC efflux pumps (ABCB1, ABCB5, ABCB8, ABCC1, ABCC2, ABCG1, and ABCG2) reportedly associated with melanoma drug resistance in different human melanoma cells and tested the efficacy of five different anti-cancer compounds (cisplatin, doxorubicin, oridonin, paclitaxel, vemurafenib) with decreased GH action. We found that GH treatment of human melanoma cells upregulates expression of multiple ABC transporters and increases the EC50 of melanoma drug vemurafenib. Also, vemurafenib-resistant melanoma cells had upregulated levels of GH receptor (GHR) expression as well as ABC efflux pumps. GHR knockdown (KD) using siRNA in human melanoma cells treated with sub-EC50 doses of anti-tumor compounds resulted in significantly increased drug retention, decreased cell proliferation and increased drug efficacy, compared to mock-transfected controls. Our set of findings identify an unknown mechanism of GH regulation in mediating melanoma drug resistance and validates GHR as a unique therapeutic target for sensitizing highly therapy-resistant human melanoma cells to lower doses of anti-cancer drugs.

Keywords

Melanoma Paclitaxel Melanoma Cell Efflux Pump Melanoma Cell Line 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Funding

This work was supported in part by the State of Ohio’s Eminent Scholar Program that includes a gift from Milton and Lawrence Goll, by the AMVETS, and the Edison Biotechnology Institute at Ohio University.

Supplementary material

12672_2017_292_MOESM1_ESM.pptx (3.7 mb)
ESM 1 (PPTX 3776 kb)

References

  1. 1.
    Welch HG (2005) Skin biopsy rates and incidence of melanoma: population based ecological study. BMJ 331:481. doi: 10.1136/bmj.38516.649537.E0 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Linos E, Swetter SM, Cockburn MG, Colditz GA, Clarke CA (2009) Increasing burden of melanoma in the United States. J. Invest. Dermatol. 129:1666–1674. doi: 10.1038/jid.2008.423 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Hery C, Tryggvadottir L, Sigurdsson T, Olafsdottir E, Sigurgeirsson B, Jonasson JG, Olafsson JH, Boniol M, Byrnes GB, Dore J-F, Autier P (2010) A melanoma epidemic in Iceland: possible influence of sunbed use. Am J Epidemiol 172:762–767. doi: 10.1093/aje/kwq238 CrossRefPubMedGoogle Scholar
  4. 4.
    Geller AC, Clapp RW, Sober AJ, Gonsalves L, Mueller L, Christiansen CL, Shaikh W, Miller DR (2013) Melanoma epidemic: an analysis of six decades of data from the Connecticut Tumor Registry. J Clin Oncol 31:4172–4178. doi: 10.1200/JCO.2012.47.3728 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Hallberg Ö, Johansson O (2013) Increasing melanoma—too many skin cell damages or too few repairs? Cancers (Basel) 5:184–204. doi: 10.3390/cancers5010184 CrossRefGoogle Scholar
  6. 6.
    Lowe GC, Saavedra A, Reed KB, Velazquez AI, Dronca RS, Markovic SN, Lohse CM, Brewer JD (2014) Increasing incidence of melanoma among middle-aged adults: an epidemiologic study in Olmsted County, Minnesota. Mayo Clin Proc 89:52–59. doi: 10.1016/j.mayocp.2013.09.014 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Berwick M (2010) Invited commentary: a sunbed epidemic? Am J Epidemiol 172:768–770. doi: 10.1093/aje/kwq232 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Boniol M, Autier P, Boyle P, Gandini S (2012) Cutaneous melanoma attributable to sunbed use: systematic review and meta-analysis. BMJ 345:e4757–e4757. doi: 10.1136/bmj.e4757 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Handler MZ, Ross AL, Shiman MI, Elgart GW, Grichnik JM (2012) Potential role of human growth hormone in melanoma growth promotion. Arch Dermatol 148:1179. doi: 10.1001/archdermatol.2012.2149 CrossRefPubMedGoogle Scholar
  10. 10.
    Ozao-Choy J, Lee DJ, Faries MB (2014) Melanoma vaccines. Surg Clin North Am 94:1017–1030. doi: 10.1016/j.suc.2014.07.005 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Zitvogel L, Kroemer G (2012) Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology 1:1223–1225. doi: 10.4161/onci.21335 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Khattak M, Fisher R, Turajlic S, Larkin J (2013) Targeted therapy and immunotherapy in advanced melanoma: an evolving paradigm. Ther Adv Med Oncol 5:105–118. doi: 10.1177/1758834012466280 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    N. Comfere, Chakraborty, Wieland, Molecular targeted therapies in metastatic melanoma, Pharmgenomics Pers Med (2013) 6:49. doi: 10.2147/PGPM.S44800.
  14. 14.
    McDermott D, Srivastava N (2014) Update on benefit of immunotherapy and targeted therapy in melanoma: the changing landscape. Cancer Manag Res 279. doi: 10.2147/CMAR.S64979
  15. 15.
    Luke JJ, Ott PA (2015) PD-1 pathway inhibitors: the next generation of immunotherapy for advanced melanoma. Oncotarget 6:3479–3492. doi: 10.18632/oncotarget.2980 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Adam D, Rajakulendran T (2015) Spotlight on pembrolizumab in the treatment of advanced melanoma. Drug Des Devel Ther 2883. doi: 10.2147/DDDT.S78036
  17. 17.
    Russo A, Ficili B, Candido S, Pezzino F, Guarneri C, Biondi A, Travali S, McCubrey J, Spandidos D, Libra M (2014) Emerging targeted therapies for melanoma treatment (review). Int. J, Oncol. doi: 10.3892/ijo.2014.2481 Google Scholar
  18. 18.
    Drake WM, Grossman AB, Hutson RK (2005) Effect of treatment with pegvisomant on meningioma growth in vivo. Eur J Endocrinol 152:161–162. doi: 10.1530/eje.1.01825 CrossRefPubMedGoogle Scholar
  19. 19.
    Liedert B, Materna V, Schadendorf D, Thomale J, Lage H (2003) Overexpression of cMOAT (MRP2/ABCC2) is associated with decreased formation of platinum-DNA adducts and decreased G2-arrest in melanoma cells resistant to cisplatin. J Invest Dermatol 121:172–176. doi: 10.1046/j.1523-1747.2003.12313.x CrossRefPubMedGoogle Scholar
  20. 20.
    Heerboth S, Housman G, Leary M, Longacre M, Byler S, Lapinska K, Willbanks A, Sarkar S (2015) EMT and tumor metastasis. Clin Transl Med 4:6. doi: 10.1186/s40169-015-0048-3 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Hernandez-Davies JE, Tran TQ, Reid MA, Rosales KR, Lowman XH, Pan M, Moriceau G, Yang Y, Wu J, Lo RS, Kong M (2015) Vemurafenib resistance reprograms melanoma cells towards glutamine dependence. J Transl Med 13:210. doi: 10.1186/s12967-015-0581-2 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Thang ND, Nghia PT, Kumasaka MY, Yajima I, Kato M (2015) Treatment of vemurafenib-resistant SKMEL-28 melanoma cells with paclitaxel. Asian Pac J Cancer Prev 16:699–705 http://www.ncbi.nlm.nih.gov/pubmed/25684511 (accessed September 26, 2016)CrossRefPubMedGoogle Scholar
  23. 23.
    Bu X, Mahoney KM, Freeman GJ (2016) Learning from PD-1 resistance: new combination strategies. Trends Mol Med 22:448–451. doi: 10.1016/j.molmed.2016.04.008 CrossRefPubMedGoogle Scholar
  24. 24.
    Zaretsky JM, Garcia-Diaz A, Shin DS, Escuin-Ordinas H, Hugo W, Hu-Lieskovan S, Torrejon DY, Abril-Rodriguez G, Sandoval S, Barthly L, Saco J, Homet Moreno B, Mezzadra R, Chmielowski B, Ruchalski K, Shintaku IP, Sanchez PJ, Puig-Saus C, Cherry G, Seja E, Kong X, Pang J, Berent-Maoz B, Comin-Anduix B, Graeber TG, Tumeh PC, Schumacher TNM, Lo RS, Ribas A (2016) Mutations associated with acquired resistance to PD-1 blockade in melanoma. N Engl J Med 375:819–829. doi: 10.1056/NEJMoa1604958 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJM, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, West AN, Carmona M, Kivork C, Seja E, Cherry G, Gutierrez AJ, Grogan TR, Mateus C, Tomasic G, Glaspy JA, Emerson RO, Robins H, Pierce RH, Elashoff DA, Robert C, Ribas A (2014) PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515:568–571. doi: 10.1038/nature13954 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Luke JJ, Hodi FS (2013) Ipilimumab, vemurafenib, dabrafenib, and trametinib: synergistic competitors in the clinical management of BRAF mutant malignant melanoma. Oncologist 18:717–725. doi: 10.1634/theoncologist.2012-0391 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Elliott AM, Al-Hajj MA (2009) ABCB8 mediates doxorubicin resistance in melanoma cells by protecting the mitochondrial genome. Mol Cancer Res 7:79–87. doi: 10.1158/1541-7786.MCR-08-0235 CrossRefPubMedGoogle Scholar
  28. 28.
    Chen KG, Valencia JC, Gillet J-P, Hearing VJ, Gottesman MM (2009) Involvement of ABC transporters in melanogenesis and the development of multidrug resistance of melanoma. Pigment Cell Melanoma Res. 22:740–749. doi: 10.1111/j.1755-148X.2009.00630.x CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Walsh N, Kennedy S, Larkin AM, Tryfonopoulos D, Eustace AJ, Mahgoub T, Conway C, Oglesby I, Collins D, Ballot J, Ooi WS, Gullo G, Clynes M, Crown J, O’Driscoll L (2010) Membrane transport proteins in human melanoma: associations with tumour aggressiveness and metastasis. Br J Cancer 102:1157–1162. doi: 10.1038/sj.bjc.6605590 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Lackner MR, Wilson TR, Settleman J (2012) Mechanisms of acquired resistance to targeted cancer therapies. Future Oncol 8:999–1014. doi: 10.2217/fon.12.86 CrossRefPubMedGoogle Scholar
  31. 31.
    Fischer KR, Durrans A, Lee S, Sheng J, Li F, Wong STC, Choi H, El Rayes T, Ryu S, Troeger J, Schwabe RF, Vahdat LT, Altorki NK, Mittal V, Gao D (2015) Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature 527:472–476. doi: 10.1038/nature15748 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Mitra A, Mishra L, Li S (2015) EMT, CTCs and CSCs in tumor relapse and drug-resistance. Oncotarget 6:10697–10711. doi: 10.18632/oncotarget.4037 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Zatelli MC, Minoia M, Molè D, Cason V, Tagliati F, Margutti A, Bondanelli M, Ambrosio MR, degli Uberti E (2009) Growth hormone excess promotes breast cancer chemoresistance. J Clin Endocrinol Metab 94:3931–3938. doi: 10.1210/jc.2009-1026 CrossRefPubMedGoogle Scholar
  34. 34.
    Perry JK, Mohankumar KM, Emerald BS, Mertani HC, Lobie PE (2008) The contribution of growth hormone to mammary neoplasia. J Mammary Gland Biol Neoplasia 13:131–145. doi: 10.1007/s10911-008-9070-z CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Pandey V, Perry JK, Mohankumar KM, Kong X-J, Liu S-M, Wu Z-S, Mitchell MD, Zhu T, Lobie PE (2008) Autocrine human growth hormone stimulates oncogenicity of endometrial carcinoma cells. Endocrinology 149:3909–3919. doi: 10.1210/en.2008-0286 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Bougen NM, Steiner M, Pertziger M, Banerjee A, Brunet-Dunand SE, Zhu T, Lobie PE, Perry JK (2012) Autocrine human GH promotes radioresistance in mammary and endometrial carcinoma cells. Endocr Relat Cancer 19:625–644. doi: 10.1530/ERC-12-0042 CrossRefPubMedGoogle Scholar
  37. 37.
    Zhang W, Qian P, Zhang X, Zhang M, Wang H, Wu M, Kong X, Tan S, Ding K, Perry JK, Wu Z, Cao Y, Lobie PE, Zhu T (2015) Autocrine/paracrine human growth hormone-stimulated MicroRNA 96-182-183 cluster promotes epithelial-mesenchymal transition and invasion in breast cancer. J Biol Chem 290:13812–13829. doi: 10.1074/jbc.M115.653261 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Wyatt D (1999) Melanocytic nevi in children treated with growth hormone. Pediatrics 104:1045–1050PubMedGoogle Scholar
  39. 39.
    Caldarola G, Battista C, Pellicano R (2010) Melanoma onset after estrogen, thyroid, and growth hormone replacement therapy. Clin Ther 32:57–59. doi: 10.1016/j.clinthera.2010.01.011 CrossRefPubMedGoogle Scholar
  40. 40.
    Lincoln DT, Sinowatz F, Kolle S, Takahashi H, Parsons P, Waters M (1999) Up-regulation of growth hormone receptor immunoreactivity in human melanoma. Anticancer Res 19:1919–1931PubMedGoogle Scholar
  41. 41.
    Sustarsic EG, Junnila RK, Kopchick JJ (2013) Human metastatic melanoma cell lines express high levels of growth hormone receptor and respond to GH treatment. Biochem Biophys Res Commun 441:144–150. doi: 10.1016/j.bbrc.2013.10.023 CrossRefPubMedGoogle Scholar
  42. 42.
    Basu R, Wu S, Kopchick J (2017) Targeting growth hormone receptor in human melanoma cells attenuates tumor progression and epithelial mesenchymal transition via suppression of multiple oncogenic pathways. Oncotarget 5. doi: 10.18632/oncotarget.15375
  43. 43.
    Vergani E, Vallacchi V, Frigerio S, Deho P, Mondellini P, Perego P, Cassinelli G, Lanzi C, Testi MA, Rivoltini L, Bongarzone I, Rodolfo M (2011) Identification of MET and SRC activation in melanoma cell lines showing primary resistance to PLX4032. Neoplasia 13:1132–IN17. doi: 10.1593/neo.111102 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Boone B, Jacobs K, Ferdinande L, Taildeman J, Lambert J, Peeters M, Bracke M, Pauwels P, Brochez L (2011) EGFR in melanoma: clinical significance and potential therapeutic target. J Cutan Pathol 38:492–502. doi: 10.1111/j.1600-0560.2011.01673.x CrossRefPubMedGoogle Scholar
  45. 45.
    Girotti MR, Pedersen M, Sanchez-Laorden B, Viros A, Turajlic S, Niculescu-Duvaz D, Zambon A, Sinclair J, Hayes A, Gore M, Lorigan P, Springer C, Larkin J, Jorgensen C, Marais R (2013) Inhibiting EGF receptor or SRC family kinase signaling overcomes BRAF inhibitor resistance in melanoma. Cancer Discov 3:158–167. doi: 10.1158/2159-8290.CD-12-0386 CrossRefPubMedGoogle Scholar
  46. 46.
    Goetz EM, Ghandi M, Treacy DJ, Wagle N, Garraway LA (2014) ERK mutations confer resistance to mitogen-activated protein kinase pathway inhibitors. Cancer Res 74:7079–7089. doi: 10.1158/0008-5472.CAN-14-2073 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Kim H, Frederick DT, Levesque MP, Cooper ZA, Feng Y, Krepler C, Brill L, Samuels Y, Hayward NK, Perlina A, Piris A, Zhang T, Halaban R, Herlyn MM, Brown KM, Wargo JA, Dummer R, Flaherty KT, Ronai ZA (2015) Downregulation of the ubiquitin ligase RNF125 underlies resistance of melanoma cells to BRAF inhibitors via JAK1 deregulation. Cell Rep 11:1458–1473. doi: 10.1016/j.celrep.2015.04.049 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Zhao C, Li H, Lin H-J, Yang S, Lin J, Liang G (2016) Feedback activation of STAT3 as a cancer drug-resistance mechanism. Trends Pharmacol Sci 37:47–61. doi: 10.1016/j.tips.2015.10.001 CrossRefPubMedGoogle Scholar
  49. 49.
    Heynen GJ, Fonfara A, Bernards R (2014) Resistance to targeted cancer drugs through hepatocyte growth factor signaling. Cell Cycle 13:3808–3817. doi: 10.4161/15384101.2014.988033 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Ma J, Lyu H, Huang J, Liu B (2014) Targeting of erbB3 receptor to overcome resistance in cancer treatment. Mol Cancer 13:105. doi: 10.1186/1476-4598-13-105 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Fattore L, Malpicci D, Marra E, Camerlingo R, Roscilli G, Belleudi F, Ribas A, Mancini R, Torrisi M, Aurisicchio L, Ascierto P, Ciliberto G (2015) ErbB3 plays a key role in the early phase of establishment of resistance to BRAF and/or MEK inhibitors. J Transl Med 13:K3. doi: 10.1186/1479-5876-13-S1-K3 CrossRefPubMedCentralGoogle Scholar
  52. 52.
    Cao H-H, Cheng C-Y, Su T, Fu X-Q, Guo H, Li T, Tse AK-W, Kwan H-Y, Yu H, Yu Z-L (2015) Quercetin inhibits HGF/c-Met signaling and HGF-stimulated melanoma cell migration and invasion. Mol Cancer 14:103. doi: 10.1186/s12943-015-0367-4 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Kim HR, Kim WS, Choi YJ, Choi CM, Rho JK, Lee JC (2013) Epithelial-mesenchymal transition leads to crizotinib resistance in H2228 lung cancer cells with EML4-ALK translocation. Mol Oncol 7:1093–1102. doi: 10.1016/j.molonc.2013.08.001 CrossRefPubMedGoogle Scholar
  54. 54.
    Du B, Shim J (2016) Targeting epithelial–mesenchymal transition (EMT) to overcome drug resistance in cancer. Molecules 21:965. doi: 10.3390/molecules21070965 CrossRefGoogle Scholar
  55. 55.
    Mallini P, Lennard T, Kirby J, Meeson A (2014) Epithelial-to-mesenchymal transition: what is the impact on breast cancer stem cells and drug resistance. Cancer Treat Rev 40:341–348. doi: 10.1016/j.ctrv.2013.09.008 CrossRefPubMedGoogle Scholar
  56. 56.
    Liang S-Q, Marti TM, Dorn P, Froment L, Hall SRR, Berezowska S, Kocher G, Schmid RA, Peng R-W (2015) Blocking the epithelial-to-mesenchymal transition pathway abrogates resistance to anti-folate chemotherapy in lung cancer. Cell Death Dis 6:e1824. doi: 10.1038/cddis.2015.195 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    McDermott M, Eustace AJ, Busschots S, Breen L, Crown J, Clynes M, O’Donovan N, Stordal B (2014) In vitro development of chemotherapy and targeted therapy drug-resistant cancer cell lines: a practical guide with case studies. Front Oncol 4. doi: 10.3389/fonc.2014.00040
  58. 58.
    Aksamitiene E, Hoek JB, Kholodenko B, Kiyatkin A (2007) Multistrip western blotting to increase quantitative data output. Electrophoresis 28:3163–3173. doi: 10.1002/elps.200700002 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    T.L. Riss, R.A. Moravec, A.L. Niles, S. Duellman, H.A. Benink, T.J. Worzella, L. Minor, Cell viability assays, 2004. http://www.ncbi.nlm.nih.gov/pubmed/23805433.Google Scholar
  60. 60.
    Riss TL, Moravec RA, Niles AL (2011) Cytotoxicity testing: measuring viable cells, dead cells, and detecting mechanism of cell death. Methods Mol Biol 740:103–114. doi: 10.1007/978-1-61779-108-6_12 CrossRefPubMedGoogle Scholar
  61. 61.
    Borra RC, Lotufo MA, Gagioti SM, Barros FDM, Andrade PM (2009) A simple method to measure cell viability in proliferation and cytotoxicity assays. Braz Oral Res 23:255–262. doi: 10.1590/S1806-83242009000300006 CrossRefPubMedGoogle Scholar
  62. 62.
    Tiberghien F, Loor F (1996) Ranking of P-glycoprotein substrates and inhibitors by a calcein-AM fluorometry screening assay. Anti-Cancer Drugs 7:568–578. doi: 10.1097/00001813-199607000-00012 CrossRefPubMedGoogle Scholar
  63. 63.
    Schonk DM, Kuijpers HJ, van Drunen E, van Dalen CH, Geurts van Kessel AH, Verheijen R, Ramaekers FC (1989) Assignment of the gene(s) involved in the expression of the proliferation-related Ki-67 antigen to human chromosome 10. Hum Genet 83:297–299 http://www.ncbi.nlm.nih.gov/pubmed/2571566 CrossRefPubMedGoogle Scholar
  64. 64.
    Heimerl S, Bosserhoff AK, Langmann T, Ecker J, Schmitz G (2007) Mapping ATP-binding cassette transporter gene expression profiles in melanocytes and melanoma cells. Melanoma Res 17:265–273. doi: 10.1097/CMR.0b013e3282a7e0b9 CrossRefPubMedGoogle Scholar
  65. 65.
    Pan S-T, Li Z-L, He Z-X, Qiu J-X, Zhou S-F (2016) Molecular mechanisms for tumour resistance to chemotherapy. Clin Exp Pharmacol Physiol 43:723–737. doi: 10.1111/1440-1681.12581 CrossRefPubMedGoogle Scholar
  66. 66.
    Landreville S, Agapova OA, Kneass ZT, Salesse C, William Harbour J (2011) ABCB1 identifies a subpopulation of uveal melanoma cells with high metastatic propensity. Pigment Cell Melanoma Res 24:430–437. doi: 10.1111/j.1755-148X.2011.00841.x CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Chartrain M, Riond J, Stennevin A, Vandenberghe I, Gomes B, Lamant L, Meyer N, Gairin JE, Guilbaud N, Annereau JP (2012) Melanoma chemotherapy leads to the selection of ABCB5-expressing cells. PLoS One 7:e36762. doi: 10.1371/journal.pone.0036762 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Wilson BJ, Saab KR, Ma J, Schatton T, Putz P, Zhan Q, Murphy GF, Gasser M, Waaga-Gasser AM, Frank NY, Frank MH (2014) ABCB5 maintains melanoma-initiating cells through a proinflammatory cytokine signaling circuit. Cancer Res 74:4196–4207. doi: 10.1158/0008-5472.CAN-14-0582 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Michaelis M, Rothweiler F, Nerreter T, van Rikxoort M, Zehner R, Dirks WG, Wiese M, Cinatl J (2014a) Association between acquired resistance to PLX4032 (vemurafenib) and ATP-binding cassette transporter expression. BMC Res Notes 7:710. doi: 10.1186/1756-0500-7-710 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Sag D, Cekic C, Wu R, Linden J, Hedrick CC (2015) The cholesterol transporter ABCG1 links cholesterol homeostasis and tumour immunity. Nat Commun 6:6354. doi: 10.1038/ncomms7354 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Ejendal KF, Hrycyna CA (2002) Multidrug resistance and cancer: the role of the human ABC transporter ABCG2. Curr Protein Pept Sci 3:503–511CrossRefPubMedGoogle Scholar
  72. 72.
    Brunet-Dunand SE, Vouyovitch C, Araneda S, Pandey V, Vidal LJ-P, Print C, Mertani HC, Lobie PE, Perry JK (2009) Autocrine human growth hormone promotes tumor angiogenesis in mammary carcinoma. Endocrinology 150:1341–1352. doi: 10.1210/en.2008-0608 CrossRefPubMedGoogle Scholar
  73. 73.
    Wu Z-S, Yang K, Wan Y, Qian P-X, Perry JK, Chiesa J, Mertani HC, Zhu T, Lobie PE (2011) Tumor expression of human growth hormone and human prolactin predict a worse survival outcome in patients with mammary or endometrial carcinoma. J Clin Endocrinol Metab 96:E1619–E1629. doi: 10.1210/jc.2011-1245 CrossRefPubMedGoogle Scholar
  74. 74.
    Perry JK, Emerald BS, Mertani HC, Lobie PE (2006) The oncogenic potential of growth hormone. Growth Hormon IGF Res 16:277–289. doi: 10.1016/j.ghir.2006.09.006 CrossRefGoogle Scholar
  75. 75.
    Fletcher JI, Haber M, Henderson MJ, Norris MD (2010) ABC transporters in cancer: more than just drug efflux pumps. Nat Rev Cancer 10:147–156. doi: 10.1038/nrc2789 CrossRefPubMedGoogle Scholar
  76. 76.
    Santisteban M (2010) ABC transporters as molecular effectors of pancreatic oncogenic pathways: the hedgehog-GLI model. J Gastrointest Cancer 41:153–158. doi: 10.1007/s12029-010-9144-1 CrossRefPubMedGoogle Scholar
  77. 77.
    Michaelis M, Rothweiler F, Nerreter T, Van Rikxoort M, Sharifi M, Wiese M, Ghafourian T, Cinatl J (2014b) Differential effects of the oncogenic BRAF inhibitor PLX4032 (vemurafenib) and its progenitor PLX4720 on ABCB1 function. J Pharm Pharm Sci 17:154–168 http://www.ncbi.nlm.nih.gov/pubmed/24735766 CrossRefPubMedGoogle Scholar
  78. 78.
    Li S, Zhang W, Yin X, Xing S, Xie HQ, Cao Z, Zhao B (2015) Mouse ATP-binding cassette (ABC) transporters conferring multi-drug resistance. Anti Cancer Agents Med Chem 15:423–432 http://www.ncbi.nlm.nih.gov/pubmed/25929575 CrossRefGoogle Scholar
  79. 79.
    Nakanishi T, Ross DD (2012) Breast cancer resistance protein (BCRP/ABCG2): its role in multidrug resistance and regulation of its gene expression. Chin J Cancer 31:73–99. doi: 10.5732/cjc.011.10320 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Wouters J, Stas M, Gremeaux L, Govaere O, Van den Broeck A, Maes H, Agostinis P, Roskams T, van den Oord JJ, Vankelecom H (2013) The human melanoma side population displays molecular and functional characteristics of enriched chemoresistance and tumorigenesis. PLoS One 8:e76550. doi: 10.1371/journal.pone.0076550 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Hayashi AA, Proud CG (2007) The rapid activation of protein synthesis by growth hormone requires signaling through mTOR. AJP Endocrinol Metab 292:E1647–E1655. doi: 10.1152/ajpendo.00674.2006 CrossRefGoogle Scholar
  82. 82.
    Jin S, Scotto KW (1998) Transcriptional regulation of the MDR1 gene by histone acetyltransferase and deacetylase is mediated by NF-Y. Mol Cell Biol 18:4377–4384 http://www.ncbi.nlm.nih.gov/pubmed/9632821 CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Scotto KW (2003) Transcriptional regulation of ABC drug transporters. Oncogene 22:7496–7511. doi: 10.1038/sj.onc.1206950 CrossRefPubMedGoogle Scholar
  84. 84.
    Oldfield AJ, Yang P, Conway AE, Cinghu S, Freudenberg JM, Yellaboina S, Jothi R (2014) Histone-fold domain protein NF-Y promotes chromatin accessibility for cell type-specific master transcription factors. Mol Cell 55:708–722. doi: 10.1016/j.molcel.2014.07.005 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Subramanian A, Wang J, Gil G (1998) STAT 5 and NF-Y are involved in expression and growth hormone-mediated sexually dimorphic regulation of cytochrome P450 3A10/lithocholic acid 6beta-hydroxylase. Nucleic Acids Res 26:2173–2178 http://www.ncbi.nlm.nih.gov/pubmed/9547277 CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Kopchick JJ, List EO, Kelder B, Gosney ES, Berryman DE (2014) Evaluation of growth hormone (GH) action in mice: discovery of GH receptor antagonists and clinical indications. Mol Cell Endocrinol 386:34–45. doi: 10.1016/j.mce.2013.09.004 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Edison Biotechnology Institute, Konneker Research Laboratory 206Ohio UniversityAthensUSA
  2. 2.Molecular and Cell Biology ProgramOhio UniversityAthensUSA
  3. 3.Department of Biological SciencesOhio UniversityAthensUSA
  4. 4.Heritage College of Osteopathic MedicineAthensUSA

Personalised recommendations