Tumor-derived hydrogen sulfide, produced by cystathionine-β-synthase, stimulates bioenergetics, cell proliferation, and angiogenesis in colon cancer

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

Volumn 110, Issue 30, 2013, Pages 12474-12479

  Szabo, Csaba ^a   Coletta, Ciro ^a   Chao, Celia ^a   Módis, Katalin ^a   Szczesny, Bartosz ^a   Papapetropoulos, Andreas ^a   Hellmich, Mark R ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINOOXYACETIC ACID; CYSTATHIONINE; CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; CYSTEINE; HYDROGEN SULFIDE; SHORT HAIRPIN RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CELL ENERGY; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL STRAIN HCT116; CELL STRAIN HT29; COCULTURE; COLON ADENOCARCINOMA; COLON CANCER; COLORECTAL CANCER; CONTROLLED STUDY; CYTOSOL; ENDOTHELIUM CELL; GENE SILENCING; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MOUSE; MUCOSA CELL; NONHUMAN; OXYGEN CONSUMPTION; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; TUMOR BLOOD FLOW; TUMOR CELL; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; TURNOVER TIME; UPREGULATION;

ANIMALS; CELL PROLIFERATION; COLONIC NEOPLASMS; CYSTATHIONINE BETA-SYNTHASE; ENERGY METABOLISM; FEMALE; HT29 CELLS; HUMANS; HYDROGEN SULFIDE; MICE; MICE, INBRED BALB C; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84880690612     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1306241110     Document Type: Article

References (47)

1. Yang G, et al. (2008) H2S as a physiologic vasorelaxant: Hypertension in mice with deletion of cystathionine gamma-lyase. Science 322(5901):587-590.
2. Mustafa AK, et al. (2011) Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ Res 109(11):1259-1268.
3. Coletta C, et al. (2012) Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci USA 109(23):9161-9166.
4. Cai WJ, et al. (2007) The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc Res 76(1):29-40.
5. Papapetropoulos A, et al. (2009) Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci USA 106(51):21972-21977.
6. Goubern M, Andriamihaja M, Nübel T, Blachier F, Bouillaud F (2007) Sulfide, the first inorganic substrate for human cells. FASEB J 21(8):1699-1706.
7. Módis K, Coletta C, Erdélyi K, Papapetropoulos A, Szabo C (2013) Intramitochondrial hydrogen sulfide production by 3-mercaptopyruvate sulfurtransferase maintains mitochondrial electron flow and supports cellular bioenergetics. FASEB J 27(2):601-611.
8. Szabo C (2007) Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6(11):917-935.
9. Kimura H (2011) Hydrogen sulfide: Its production, release and functions. Amino Acids 41(1):113-121.
10. Li L, Rose P, Moore PK (2011) Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 51:169-187.
11. Cai WJ, Wang MJ, Ju LH, Wang C, Zhu YC (2010) Hydrogen sulfide induces human colon cancer cell proliferation: Role of Akt, ERK and p21. Cell Biol Int 34(6):565-572.
12. Manna P, Jain SK (2011) Hydrogen sulfide and L-cysteine increase phosphatidylinositol 3,4,5-trisphosphate (PIP3) and glucose utilization by inhibiting phosphatase and tensin homolog (PTEN) protein and activating phosphoinositide 3-kinase (PI3K)/serine/threonine protein kinase (AKT)/protein kinase C?/? (PKC?/?) in 3T3l1 adipocytes. J Biol Chem 286(46):39848-39859.
13. Bucci M, et al. (2010) Hydrogen sulfide is an endogenous inhibitor of phosphodiesterase activity. Arterioscler Thromb Vasc Biol 30(10):1998-2004.
14. Mustafa AK, et al. (2009) H2S signals through protein S-sulfhydration. Sci Signal 2(96): Ra72.
15. Paul BD, Snyder SH (2012) H2S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol 13(8):499-507.
16. Mathupala SP, Ko YH, Pedersen PL (2010) The pivotal roles of mitochondria in cancer: Warburg and beyond and encouraging prospects for effective therapies. Biochim Biophys Acta 1797(6-7):1225-1230.
17. Schulze A, Harris AL (2012) How cancer metabolism is tuned for proliferation and vulnerable to disruption. Nature 491(7424):364-373.
18. Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473(7347):298-307.
19. Cook KM, Figg WD (2010) Angiogenesis inhibitors: Current strategies and future prospects. CA Cancer J Clin 60(4):222-243.
20. Lagoutte E, et al. (2010) Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim Biophys Acta 1797(8):1500-1511.
21. Mimoun S, et al. (2012) Detoxification of H(2)S by differentiated colonic epithelial cells: Implication of the sulfide oxidizing unit and of the cell respiratory capacity. Antioxid Redox Signal 17(1):1-10.
22. Tentler JJ, et al. (2012) Patient-derived tumour xenografts as models for oncology drug development. Nat Rev Clin Oncol 9(6):338-350.
23. Krishnan N, Fu C, Pappin DJ, Tonks NK (2011) H2S-induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci Signal 4(203):ra86.
24. Deplancke B, Gaskins HR (2003) Hydrogen sulfide induces serum-independent cell cycle entry in nontransformed rat intestinal epithelial cells. FASEB J 17(10):1310-1312.
25. Szabo C, Papapetropoulos A (2011) Hydrogen sulphide and angiogenesis: Mechanisms and applications. Br J Pharmacol 164(3):853-865.
26. Qipshidze N, Metreveli N, Mishra PK, Lominadze D, Tyagi SC (2012) Hydrogen sulfide mitigates cardiac remodeling during myocardial infarction via improvement of angiogenesis. Int J Biol Sci 8(4):430-441.
27. Pupo E, et al. (2011) Hydrogen sulfide promotes calcium signals and migration in tumor-derived endothelial cells. Free Radic Biol Med 51(9):1765-1773.
28. Lee ZW, et al. (2011) The slow-releasing hydrogen sulfide donor, GYY4137, exhibits novel anti-cancer effects in vitro and in vivo. PLoS ONE 6(6):e21077.
29. Wu YC, et al. (2012) Hydrogen sulfide lowers proliferation and induces protective autophagy in colon epithelial cells. PLoS ONE 7(5):e37572.
30. Baskar R, Bian J (2011) Hydrogen sulfide gas has cell growth regulatory role. Eur J Pharmacol 656(1-3):5-9.
31. Yamagishi K, et al. (2012) Generation of gaseous sulfur-containing compounds in tumour tissue and suppression of gas diffusion as an antitumour treatment. Gut 61(4):554-561.
32. Kumar S, et al. (2012) Selected ion flow tube-MS analysis of headspace vapor from gastric content for the diagnosis of gastro-esophageal cancer. Anal Chem 84(21): 9550-9557.
33. De Vos J, et al. (2002) Comparison of gene expression profiling between malignant and normal plasma cells with oligonucleotide arrays. Oncogene 21(44):6848-6857.
34. Hansel DE, et al. (2003) Identification of novel cellular targets in biliary tract cancers using global gene expression technology. Am J Pathol 163(1):217-229.
35. Guo H, et al. (2012) Characterization of hydrogen sulfide and its synthases, cystathionine β-synthase and cystathionine ?-lyase, in human prostatic tissue and cells. Urology. 79:483.e1-5.
36. Thornburg JM, et al. (2008) Targeting aspartate aminotransferase in breast cancer. Breast Cancer Res 10(5):R84.
37. Perry TL, et al. (1980) Failure of aminooxyacetic acid therapy in Huntington disease. Neurology 30(7 Pt 1):772-775.
38. Turski WA, Dziki M, Urbanska E, Calderazzo-Filho LS, Cavalheiro EA (1991) Seizures induced by aminooxyacetic acid in mice: Pharmacological characteristics. Synapse 7(3): 173-180.
39. Støttrup NB, et al. (2010) Inhibition of the malate-aspartate shuttle by pre-ischaemic aminooxyacetate loading of the heart induces cardioprotection. Cardiovasc Res 88(2): 257-266.
40. Chao C, et al. (2010) CCK2 receptor expression transforms non-tumorigenic human NCM356 colonic epithelial cells into tumor forming cells. Int J Cancer 126(4):864-875.
41. Frezza C, Cipolat S, Scorrano L (2007) Organelle isolation: Functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat Protoc 2(2):287-295.
42. Szczesny B, Hazra TK, Papaconstantinou J, Mitra S, Boldogh I (2003) Age-dependent deficiency in import of mitochondrial DNA glycosylases required for repair of oxidatively damaged bases. Proc Natl Acad Sci USA 100(19):10670-10675.
43. Módis K, Asimakopoulou A, Coletta C, Papapetropoulos A, Szabo C (2013) Oxidative stress suppresses the cellular bioenergetic effect of the 3-mercaptopyruvate sulfurtransferase/hydrogen sulfide pathway. Biochem Biophys Res Commun 433(4):401-407.
44. Kriebitzsch C, et al. (2011) 1,25-dihydroxyvitamin D3 influences cellular homocysteine levels in murine preosteoblastic MC3T3-E1 cells by direct regulation of cystathionine β-synthase. J Bone Miner Res 26(12):2991-3000.
45. Kim SO, et al. (2012) Raf-1 kinase inhibitory protein (RKIP) mediates ethanol-induced sensitization of secretagogue signaling in pancreatic acinar cells. J Biol Chem 287(40): 33377-33388.
46. Chao C, Lotz MM, Clarke AC, Mercurio AM (1996) A function for the integrin alpha6beta4 in the invasive properties of colorectal carcinoma cells. Cancer Res 56(20): 4811-4819.
47. Wu M, et al. (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol 292(1):C125-C136.