Nitric oxide regulates the expression of heme carrier protein-1 via hypoxia inducible factor-1α stabilization


Autoři: Hiromi Kurokawa aff001;  Hiromu Ito aff002;  Masahiko Terasaki aff003;  Daisuke Matano aff003;  Atsushi Taninaka aff004;  Hidemi Shigekawa aff004;  Hirofumi Matsui aff001
Působiště autorů: Faculty of Medicine, University of Tsukuba, Ibaraki, Japan aff001;  Graduate School of Medical and Dental Sciences, Kagoshima University, Kagoshima, Japan aff002;  Graduate School of Comprehensive Human Sciences, University of Tsukuba, Ibaraki, Japan aff003;  Faculty of Pure and Applied Sciences, University of Tsukuba, Ibaraki, Japan aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222074

Souhrn

Photodynamic therapy (PDT) is a cancer therapy that capitalizes on cancer-specific porphyrin accumulation. We have investigated this phenomenon to propose the following three conclusions: 1) the mechanism underlying this phenomenon is closely related to both nitric oxide (NO) and heme carrier protein-1 (HCP-1), 2) NO inactivates ferrochelatase, and thus, the intracellular porphyrin levels in the cells are increased by the administration of an NO donor after 5-aminolevulinic acid treatment, 3) HCP-1 transports not only heme but also other porphyrins. Since NO stabilizes hypoxia-inducible factor (HIF)-1α, resulting in the upregulation of heme biosynthesis, HCP-1 expression can be increased by HIF-1α stabilization. In this study, we determined whether NO regulates HCP-1 expression by stabilizing HIF-1α expression. For this purpose, rat gastric cancer cell line RGK36 was treated with L-arginine or N6-(1-iminoethyl)-L-lysine (L-NIL). L-arginine treatment increased the intracellular NO concentration, and both HCP-1 and HIF-1α expression, while L-NIL treatment decreased them. Cytotoxicity of PDT was enhanced by L-arginine, following intracellular hemato-porphyrin dihydrochloride (HpD) accumulation. Both Cytotoxicity of PDT and HpD accumulation were decreased by L-NIL. The HCP-1 and HIF-1α expression, intracellular HpD accumulation and PDT cytotoxicity were decreased by 2-methoxyestradiol, which is a HIF-1α inhibitor. Moreover, these phenomena were not increased by a combination of both L-arginine and 2-Me. Thus, HCP-1 can be a downstream target of HIF-1α. These effects were also induced in the human gastric cancer cell line MKN45. Taken together, we conclude that HCP-1 expression is regulated by NO via HIF-1α stabilization.

Klíčová slova:

Biology and life sciences – Biochemistry – Neurochemistry – Neurochemicals – Nitric oxide – Proteins – Post-translational modification – Heme – Neuroscience – Toxicology – Cytotoxicity – Physical sciences – Chemistry – Chemical compounds – Organic compounds – Porphyrins – Organic chemistry – Medicine and health sciences – Pathology and laboratory medicine – Oncology – Cancer treatment – Cancers and neoplasms – Gastrointestinal tumors – Gastric cancer – Engineering and technology – Equipment – Optical equipment – Lasers – Research and analysis methods – Electrophoretic techniques – Gel electrophoresis


Zdroje

1. Rajesh S, Koshi E, Philip K, Mohan A. Antimicrobial photodynamic therapy: An overview. J Indian Soc Periodontol. 2011; 5: 323–327.

2. Malik R, Manocha A, Suresh DK. Photodynamic therapy—a strategic review. Indian J Dent Res. 2010; 21: 285–291. doi: 10.4103/0970-9290.66659 20657102

3. Luo D, Carter KA, Miranda D, Lovell JF. Chemophototherapy: An Emerging Treatment Option for Solid Tumors. Adv Sci (Weinh). 2017; 4: 1600106.

4. Lee JY and Lim JY. The Prospect of the Fourth Industrial Revolution and Home Healthcare in Super-Aged Society. Ann Geriatr Med Res. 2017; 21: 95–100.

5. Nishiwaki Y. The Advantages of Photodynamic Therapy for Gastric Cancer in This Era of an Increasing Elderly Population–From a Surgeon’s Point of View. Nippon Laser Igakkaishi, 2015; 36: 138–145.

6. Kwiatkowski S, Knap B, Przystupski D, Saczko J, Kędzierska E, Knap-Czop K, et al. Photodynamic therapy—mechanisms, photosensitizers and combinations. Biomed Pharmacother. 2018; 106: 1098–1107. doi: 10.1016/j.biopha.2018.07.049 30119176

7. Lee JB, Choi JY, Chun JS, Yun SJ, Lee SC, Oh J, et al. Relationship of protoporphyrin IX synthesis to photodynamic effects by 5-aminolaevulinic acid and its esters on various cell lines derived from the skin. Br J Dermatol. 2008; 159: 61–67. doi: 10.1111/j.1365-2133.2008.08611.x 18489589

8. Jedrych E, Chudy M, Dybko A, Brzozka Z. The microfluidic system for studies of carcinoma and normal cells interactions after photodynamic therapy (PDT) procedures. Biomicrofluidics. 2011; 5: 41101–411016. doi: 10.1063/1.3658842 22662052

9. Shayeghi M, Latunde-Dada GO, Oakhill JS, Laftah AH, Takeuchi K, Halliday N, et al. Identification of an intestinal heme transporter. Cell. 2005; 122: 789–801. doi: 10.1016/j.cell.2005.06.025 16143108

10. Andrews NC. Understanding heme transport. The New England journal of medicine. 2005; 353: 2508–2509. doi: 10.1056/NEJMcibr053987 16339100

11. Hiyama K, Matsui H, Tamura M, Shimokawa O, Hiyama M, Kaneko T, et al. Cancer cells uptake porphyrins via heme carrier protein 1. Journal of Porphyrins and Phthalocyanines. 2012; 16: 1–8.

12. Ito H, Matsui H, Tamura M, Majima HJ, Indo HP, Hyodo I. Mitochondrial reactive oxygen species accelerate the expression of heme carrier protein 1 and enhance photodynamic cancer therapy effect. Journal of clinical biochemistry and nutrition. 2014; 55: 67–71. doi: 10.3164/jcbn.14-27 25120282

13. Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991; 43: 109–142. 1852778

14. Jadeski LC, Hum KO, Chakraborty C, Lala PK. Nitric oxide promotes murine mammary tumour growth and metastasis by stimulating tumour cell migration, invasiveness and angiogenesis. International journal of cancer. 2000; 86: 30–39. doi: 10.1002/(sici)1097-0215(20000401)86:1<30::aid-ijc5>3.0.co;2-i 10728591

15. Fukumura D, Yuan F, Endo M, Jain RK. Role of nitric oxide in tumor microcirculation. Blood flow, vascular permeability, and leukocyte-endothelial interactions. The American journal of pathology. 1997; 150: 713–725. 9033284

16. Kiziltepe T, Hideshima T, Ishitsuka K, Ocio EM, Raje N, Catley L, et al. JS-K, a GST-activated nitric oxide generator, induces DNA double-strand breaks, activates DNA damage response pathways, and induces apoptosis in vitro and in vivo in human multiple myeloma cells. Blood. 2007; 110: 709–718. doi: 10.1182/blood-2006-10-052845 17384201

17. Shupik MA, Vanin AF, Alessenko AV. Interaction of the nitric oxide signaling system with the sphingomyelin cycle and peroxidation on transmission of toxic signal of tumor necrosis factor-alpha in ischemia-reperfusion. Biochemistry (Mosc). 2011; 76: 1197–1209. doi: 10.1134/S0006297911110010 22117546.

18. Yamamoto F, Ohgari Y, Yamaki N, Kitajima S, Shimokawa O, Matsui H, et al. The role of nitric oxide in delta-aminolevulinic acid (ALA)-induced photosensitivity of cancerous cells. Biochemical and biophysical research communications. 2007; 353: 541–546. doi: 10.1016/j.bbrc.2006.12.007 17196160

19. Matsui H, Udo J, Kaneko T, Shimokawa O, Hyodo I. Nitric Oxide induces Cancer Specific Fluorescence after Aminolevulic Acid Treatment. The Journal of Japan Society for Laser Surgery and Medicine. 2008; 29: 153–159.

20. Sandau KB, Fandrey J, Brune B. Accumulation of HIF-1alpha under the influence of nitric oxide. Blood. 2001; 97: 1009–1015. doi: 10.1182/blood.v97.4.1009 11159530

21. Lin C, McGough R, Aswad B, Block JA, Terek R. Hypoxia induces HIF-1alpha and VEGF expression in chondrosarcoma cells and chondrocytes. Journal of orthopaedic research: official publication of the Orthopaedic Research Society. 2004; 22: 1175–1181.

22. Jazwa A, Stoszko M, Tomczyk M, Bukowska-Strakova K, Pichon C, Jozkowicz A, et al. HIF-regulated HO-1 gene transfer improves the post-ischemic limb recovery and diminishes TLR-triggered immune responses—Effects modified by concomitant VEGF overexpression. Vascul Pharmacol. 2015; 71: 127–138. doi: 10.1016/j.vph.2015.02.011 25869523

23. Liu YL, Ang SO, Weigent DA, Prchal JT, Bloomer JR. Regulation of ferrochelatase gene expression by hypoxia. Life sciences. 2004; 75: 2035–2043. doi: 10.1016/j.lfs.2004.03.027 15312748

24. Shimokawa O, Matsui H, Nagano Y, Kaneko T, Shibahara T, Nakahara A, et al. Neoplastic transformation and induction of H+,K+ -adenosine triphosphatase by N-methyl-N'-nitro-N-nitrosoguanidine in the gastric epithelial RGM-1 cell line. In vitro cellular & developmental biology Animal. 2008; 44: 26–30.

25. Vannini F, Kashfi K, Nath N. The dual role of iNOS in cancer. Redox biology. 2015; 6: 334–343. doi: 10.1016/j.redox.2015.08.009 26335399

26. Moore WM, Webber RK, Jerome GM, Tjoeng FS, Misko TP, Currie MG. L-N6-(1-iminoethyl)lysine: a selective inhibitor of inducible nitric oxide synthase. Journal of medicinal chemistry. 1994; 37: 3886–3888. doi: 10.1021/jm00049a007 7525961

27. Brune B, Zhou J. Nitric oxide and superoxide: interference with hypoxic signaling. Cardiovascular research. 2007; 75: 275–282. doi: 10.1016/j.cardiores.2007.03.005 17412315

28. Park YK, Ahn DR, Oh M, Lee T, Yang EG, Son M, et al. Nitric oxide donor, (+/-)-S-nitroso-N-acetylpenicillamine, stabilizes transactive hypoxia-inducible factor-1alpha by inhibiting von Hippel-Lindau recruitment and asparagine hydroxylation. Molecular pharmacology. 2008; 74: 236–245. doi: 10.1124/mol.108.045278 18426857

29. Pribluda VS, Gubish ER Jr., Lavallee TM, Treston A, Swartz GM, Green SJ. 2-Methoxyestradiol: an endogenous antiangiogenic and antiproliferative drug candidate. Cancer metastasis reviews. 2000; 19: 173–179. 11191057

30. Mabjeesh NJ, Escuin D, LaVallee TM, Pribluda VS, Swartz GM, Johnson MS, et al. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer cell. 2003; 3: 363–375. 12726862

31. Liu YL, Ang SO, Weigent DA, Prchal JT, Bloomer JR. Regulation of ferrochelatase gene expression by hypoxia. Life Sci. 2004; 75: 2035–2043. doi: 10.1016/j.lfs.2004.03.027 15312748


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden